Download PDF
Semin Thromb Hemost 2003; 29(5): 435-450
DOI: 10.1055/s-2003-44551
Copyright © 2003 by Thieme Medical Publishers, Inc., 333 Seventh Avenue, New York, NY 10001, USA. Tel.: +1(212) 584-4662

Blood Rheology and Hemodynamics

Oguz K. Baskurt1 , Herbert J. Meiselman2
  • 1Department of Physiology, Akdeniz University Faculty of Medicine, Antalya, Turkey
  • 2Professor, Department of Physiology and Biophysics, University of Southern California School of Medicine, Los Angeles, California
Further Information

Publication History

Publication Date:
21 November 2003 (online)

    Permissions and Reprints

ABSTRACT

Blood is a two-phase suspension of formed elements (i.e., red blood cells [RBCs], white blood cells [WBCs], platelets) suspended in an aqueous solution of organic molecules, proteins, and salts called plasma. The apparent viscosity of blood depends on the existing shear forces (i.e., blood behaves as a non-Newtonian fluid) and is determined by hematocrit, plasma viscosity, RBC aggregation, and the mechanical properties of RBCs. RBCs are highly deformable, and this physical property significantly contributes to aiding blood flow both under bulk flow conditions and in the microcirculation. The tendency of RBCs to undergo reversible aggregation is an important determinant of apparent viscosity because the size of RBC aggregates is inversely proportional to the magnitude of shear forces; the aggregates are dispersed with increasing shear forces, then reform under low-flow or static conditions. RBC aggregation also affects the in vivo fluidity of blood, especially in the low-shear regions of the circulatory system. Blood rheology has been reported to be altered in various physiopathological processes: (1) Alterations of hematocrit significantly contribute to hemorheological variations in diseases and in certain extreme physiological conditions; (2) RBC deformability is sensitive to local and general homeostasis, with RBC deformability affected by alterations of the properties and associations of membrane skeletal proteins, the ratio of RBC membrane surface area to cell volume, cell morphology, and cytoplasmic viscosity. Such alterations may result from genetic disorders or may be induced by such factors as abnormal local tissue metabolism, oxidant stress, and activated leukocytes; and (3) RBC aggregation is mainly determined by plasma protein composition and surface properties of RBCs, with increased plasma concentrations of acute phase reactants in inflammatory disorders a common cause of increased RBC aggregation. In addition, RBC aggregation tendency can be modified by alterations of RBC surface properties because of RBC in vivo aging, oxygen-free radicals, or proteolytic enzymes. Impairment of blood fluidity may significantly affect tissue perfusion and result in functional deteriorations, especially if disease processes also disturb vascular properties.

KEYWORDS

Hemorheology - hemodynamics - viscosity - erythrocyte deformability - erythrocyte aggregation - tissue perfusion - blood flow

REFERENCES

  • 1 Bujalkova M, Straka S, Jureckova A. Hippocrates' humoral pathology in nowaday's reflections.  Bratisl Lek Listy . 2001;  102 489-492
    PubMedGoogle Scholar
  • 2 Riddle J M. Theory and practice in medieval medicine.  Viator . 1974;  5 157-184
    PubMedGoogle Scholar
  • 3 Schultz S G. Willam Harvey and the circulation of the blood: The birth of a scientific revolution and modern physiology.  News Physiol Sci . 2002;  17 175-180
    PubMedGoogle Scholar
  • 4 Hull G. The influence of Herman Boerhaave.  J R Soc Med . 1997;  90 512-514
    PubMedGoogle Scholar
  • 5 Copley A L. Robin Fahraeus-the scientist and the person.  Clin Hemorheol . 1989;  9 395-433
    PubMedGoogle Scholar
  • 6 Bauer A. Historia magistra pathologiae.  Würzbg Medizinhist Mitt . 1993;  11 59-76
    PubMedGoogle Scholar
  • 7 Goldsmith H L, Cokelet G, Gaehtgens P. Robin Fahraeus: evolution of his concepts cardiovascular physiology.  Am J Physiol . 1989;  257 H1005-H1015
    PubMedGoogle Scholar
  • 8 Copley A L. Fluid mechanics and biorheology.  Clin Hemorheol . 1990;  10 3-19
    PubMedGoogle Scholar
  • 9 Merrill E W. Rheology of blood.  Physiol Rev . 1969;  49 863-888
    PubMedGoogle Scholar
  • 10 Matrai A, Whittington R B, Skalak R. Biophysics. In: Chien S, Dormandy J, Ernst E, Matrai A, eds. Clinical Hemorheology Dordrecht: Martinus Nijhoff 1987: 9-71
    Google Scholar
  • 11 Thurston G B. Viscoelasticity of human blood.  Biophys J . 1972;  12 1205-1217
    PubMedGoogle Scholar
  • 12 Lowe G DO, Barbenel J C. Plasma and blood viscosity. In: Lowe GDO, ed. Clinical Blood Rheology, Vol 1 Boca Raton, FL: CRC Press 1988: 11-44
    Google Scholar
  • 13 Ross J, Schmid-Schönbein G. Dynamics of the peripheral circulation. In: West JB, ed. Physiological Basis of Medical Practice Baltimore, MD: Williams & Wilkins 1990: 138-158
    Google Scholar
  • 14 Rampling M W. Red cell aggregation and yield stress. In: Lowe GDO, ed. Clinical Blood Rheology Boca Raton, FL: CRC Press 1988: 11-44
    Google Scholar
  • 15 Chien S. Biophysical behavior of red cells in suspension. In: Surgenor DM, ed. Red Blood Cell, Vol 3. New York: Academic Press 1975: 1031-1133
    Google Scholar
  • 16 Rand P W, Lacombe E, Hunt H E, Austin W H. Viscosity of normal human blood under normothermic and hypothermic conditions.  J Appl Physiol . 1964;  19 117-122
    Google Scholar
  • 17 Somer T, Meiselman H J. Disorders of blood viscosity.  Ann Med . 1993;  25 31-39
    PubMedGoogle Scholar
  • 18 Lowe G DO. Rheology of paraproteinemias and leukemias. In: Lowe GDO, ed. Clinical Blood Rheology, Vol 2 Boca Raton, FL: CRC Press 1988: 67-88
    Google Scholar
  • 19 Cokelet G R. Rheology and tube flow of blood. In: Skalak R, Chien S, eds. Handbook of Engineering New York: McGraw-Hill 1987: 14.1-14.17
    Google Scholar
  • 20 Schmid-Schönbein H, Wells R E, Goldstone J. Fluid drop-like behaviour of erythrocyte-disturbance in pathology in its quantification.  Biorheology . 1971;  7 227-234
    PubMedGoogle Scholar
  • 21 Wells R, Schmid-Schönbein H. Red cell deformation and fluidity of concentrated cell suspensions.  J Appl Physiol . 1969;  27 213-217
    PubMedGoogle Scholar
  • 22 Chien S, Sung L A. Physicochemical basis and clinical implications of red cell aggregation.  Clin Hemorheol . 1987;  7 71-91
    PubMedGoogle Scholar
  • 23 Chien S. Red cell deformability and its relevance to blood flow.  Annu Rev Physiol . 1987;  49 177-192
    PubMedGoogle Scholar
  • 24 Baskurt O K, Meiselman H J. Cellular determinants of low-shear blood viscosity.  Biorheology . 1997;  34 235-247
    CrossrefPubMedGoogle Scholar
  • 25 Lipowsky H H, Cram L E, Justice W, Eppihimer M J. Effect of erythrocyte deformability on in vivo red cell transit time and hematocrit and their correlation with in vitro filterability.  Microvasc Res . 1993;  46 43-64
    PubMedGoogle Scholar
  • 26 Mchedlishvili G, Varazashvili M, Gobejishvili L. Local RBC aggregation disturbing blood fluidity and causing stasis in microvessels.  Clin Hemorheol Microcirc . 2002;  26 99-106
    PubMedGoogle Scholar
  • 27 Eppihimer M J, Lipowsky H H. Effects of leukocyte-capillary plugging on the resistance of flow in the microvasculature of cremaster muscle for normal and activated leukocytes.  Microvasc Res . 1996;  51 187-201
    PubMedGoogle Scholar
  • 28 Mohandas N, Chasis J A. Red blood cell deformability, membrane material properties and shape: regulation by transmembrane, skeletal and cytosolic proteins and lipids.  Semin Hematol . 1993;  30 171-192
    PubMedGoogle Scholar
  • 29 Mohandas N, Chasis J A, Shohet S B. The influence of membrane skeleton on red cell deformability, membrane material properties and shape.  Semin Hematol . 1983;  20 225-242
    PubMedGoogle Scholar
  • 30 Evans E A, LaCelle P L. Intrinsic material properties of erythrocyte membrane indicated by mechanical analysis of deformation.  Blood . 1975;  45 29-43
    PubMedGoogle Scholar
  • 31 Chasis J A, Shohet S B. Red cell biochemical anatomy and membrane material properties.  Annu Rev Physiol . 1987;  49 237-248
    CrossrefPubMedGoogle Scholar
  • 32 Hochmuth R M, Waugh R. Erythrocyte membrane elasticity and viscosity.  Annu Rev Physiol . 1986;  49 209-219
    PubMedGoogle Scholar
  • 33 Lux S E. Dissecting the red cell membrane skeleton.  Nature . 1979;  281 426-429
    CrossrefPubMedGoogle Scholar
  • 34 Mohandas N, Shohet S B. The role of membrane associated enzymes in regulation of erythrocyte shape and deformability.  Clin Hematol . 1981;  10 223-237
    PubMedGoogle Scholar
  • 35 Chien S. Principles and techniques for assessing erythrocyte deformability.  Blood Cells . 1977;  3 71-95
    PubMedGoogle Scholar
  • 36 Baskurt O K, Fisher T C, Meiselman H J. Sensitivity of the cell transit analyzer (CTA) to alterations of red blood cell deformability: role of cell size-pore size ratio and sample preparation.  Clin Hemorheol . 1996;  16 753-765
    PubMedGoogle Scholar
  • 37 Hardeman M R, Goedhart P T, Dobbe J GG, Lettinga K P. Laser assisted optical rotational cell analyzer (LORCA): a new instrument for measurement of various structural hemorheological parameters.  Clin Hemorheol Microcirc . 1994;  14 605-618
    PubMedGoogle Scholar
  • 38 Meiselman H J. Red blood cell role in RBC aggregation: 1963-1993 and beyond.  Clin Hemorheol . 1993;  13 575-592
    PubMedGoogle Scholar
  • 39 Nash G B, Wenby R B, Meiselman H J. Influence of cellular factors on red cell aggregation.  Clin Hemorheol . 1987;  7 93-108
    PubMedGoogle Scholar
  • 40 Armstrong J K, Meiselman H J, Wenby R B, Fisher T C. Modulation of red blood cell aggregation and blood viscosity by the covalent attachment of Pluronic copolymers.  Biorheology . 2001;  38 239-247
    PubMedGoogle Scholar
  • 41 Baskurt O K, Temiz, A, Meiselman H J. Effect of superoxide anions on red blood cell rheologic properties.  Free Radic Biol Med . 1998;  24 102-110
    CrossrefPubMedGoogle Scholar
  • 42 Baskurt O K, Meiselman H J. Activated polymorphonuclear leukocytes affect red blood cell aggregability.  J Leukoc Biol . 1998;  63 89-93
    PubMedGoogle Scholar
  • 43 Baskurt O K, Temiz A, Meiselman H J. Red blood cell aggregation in experimental sepsis.  J Lab Clin Med . 1997;  130 183-190
    CrossrefPubMedGoogle Scholar
  • 44 Baskurt O K, Farley R A, Meiselman H J. Erythrocyte aggregation tendency and cellular properties in horse, human and rat: a comparative study.  Am J Physiol . 1997;  273 H2604-H2612
    PubMedGoogle Scholar
  • 45 Baskurt O K, Bor-Küçükatay M, Yalcin O, Meiselman H J, Armstrong J K. Standard aggregating media to test the "aggregability" of rat red blood cells.  Clin Hemorheol Microcirc . 2000;  22 161-166
    PubMedGoogle Scholar
  • 46 Kobuchi Y, Tadanao I, Ogiwara A. A model for rouleaux pattern formation of red blood cells.  J Theor Biol . 1988;  130 129-145
    PubMedGoogle Scholar
  • 47 Brooks D E, Greig R G, Janzen J. Mechanisms of erythrocyte aggregation. In: Cokelet GR, Meiselman HJ, Brooks DE, eds. Mechanisms of Erythrocyte Aggregation in Erythrocyte Mechanics and Blood Flow New York: A.R. Liss 1980: 119-140
    Google Scholar
  • 48 Chien S, Jan K M. Ultrastructural basis of the mechanism of rouleaux formation.  Microvasc Res . 1973;  5 155-166
    PubMedGoogle Scholar
  • 49 van Oss J C, Arnold K, Coakley W T. Depletion flocculation and depletion stabilization of erythrocytes.  Cell Biophys . 1990;  17 1-10
    PubMedGoogle Scholar
  • 50 Evans E, Berk D, Leung A, Mohandas N. Detachment of agglutinin-bonded red blood cells.  Biophys J . 1991;  59 849-860
    PubMedGoogle Scholar
  • 51 Baskurt O K, Tugral E, Neu B, Meiselman H J. Particle electrophoresis as a tool to understand the aggregation behavior of red blood cells.  Electrophoresis . 2002;  23 2103-2109
    CrossrefPubMedGoogle Scholar
  • 52 Neu B, Meiselman H J. Depletion-mediated red blood cell aggregation in polymer solutions.  Biophys J . 2002;  83 2482-2490
    PubMedGoogle Scholar
  • 53 Bäumler H, Donath E, Krabi A. et al . Electrophoresis of human red blood cells and platelets: evidence for depletion of dextran.  Biorheology . 1996;  33 333-351
    CrossrefPubMedGoogle Scholar
  • 54 Bäumler H, Neu B, Donath E, Kiesewetter H. Basic phenomena of red blood cell rouleaux formation.  Biorheology . 1999;  36 439-442
    PubMedGoogle Scholar
  • 55 Bauersachs R M, Wenby R B, Meiselman H J. Determination of specific red blood cell aggregation indices via an automated system.  Clin Hemorheol . 1989;  9 1-25
    PubMedGoogle Scholar
  • 56 Baskurt O K, Meiselman H J, Kayar E. Measurement of red blood cell aggregation in a "plate-plate" shearing system by analysis of light transmission.  Clin Hemorheol Microcirc . 1998;  19 307-314
    PubMedGoogle Scholar
  • 57 Firrell J C, Lipowsky H H. Leukocyte margination and deformation in mesenteric venules of rat.  Am J Physiol . 1989;  256 H1667-H1674
    PubMedGoogle Scholar
  • 58 Buttrum S M, Nash G B, Hatton R. Changes in neutrophil rheology after acute ischemia and reperfusion in the rat hindlimb.  J Lab Clin Med . 1996;  128 506-514
    CrossrefPubMedGoogle Scholar
  • 59 Buttrum S M, Drost E M, MacNee W. et al . Rheological response of neutrophils to different types of stimulation.  J Appl Physiol . 1994;  77 1801-1810
    PubMedGoogle Scholar
  • 60 Nash G B, Abbitt K B, Tate K, Jetha K A, Egginton S. Changes in the mechanical and adhesive behaviour of human neutrophils on cooling in vitro.  Pflügers Arch . 2001;  442 762-770
    PubMedGoogle Scholar
  • 61 Isbister J P. The stress polycythaemia syndromes and their haemorheological significance.  Clin Hemorheol . 1987;  7 159-179
    PubMedGoogle Scholar
  • 62 Boucher J H. The equine spleen: source of dangerous red blood cells.  J Equine Vet Sci . 1987;  7 140-142
    PubMedGoogle Scholar
  • 63 Baskurt O K, Levi E, Caglayan S. et al . The role of hemorheologic factors in the coronary circulation.  Clin Hemorheol . 1991;  11 121-127
    PubMedGoogle Scholar
  • 64 Fan F-C, Chen R YZ, Schuessler G B, Chien S. Effects of hematocrit variations on regional hemodynamics and oxygen transport in the dog.  Am J Physiol . 1980;  238 H545-H552
    PubMedGoogle Scholar
  • 65 Rendell M, Luu T, Quinlan E. et al . Red cell filterability determined using the cell transit time analyzer (CTTA): effects of ATP depletion and changes in calcium concentration.  Biochim Biophys Acta . 1992;  1133 293-300
    PubMedGoogle Scholar
  • 66 Kayar E, Mat F, Meiselman H J, Baskurt OK: Red blood cell rheological alteration in a rat model of ischemia-reperfusion injury. Biorheology .  2001;  38 405-414
    PubMedGoogle Scholar
  • 67 Mohandas N, Evans E. Mechanical properties of the red cell membrane in relation to molecular structure and genetic defects.  Annu Rev Biophys Biomol Struct . 1994;  23 787-818
    PubMedGoogle Scholar
  • 68 Shiga T, Maeda N, Kon K. Erythrocyte rheology.  Crit Rev Oncol Hematol . 1990;  10 9-48
    CrossrefPubMedGoogle Scholar
  • 69 Friederichs E, Meiselman H J. Effects of calcium permeabilization on RBC rheologic behavior.  Biorheology . 1994;  31 207-215
    PubMedGoogle Scholar
  • 70 Turchetti V, Leoncini F, De Matteis C. et al . Evaluation of erythrocyte morphology as deformability index in patients suffering from vascular diseases, with or without diabetes mellitus: correlation with blood viscosity and intra-erythrocytic calcium.  Clin Hemorheol Microcirc . 1998;  18 141-149
    PubMedGoogle Scholar
  • 71 Brun J F. Hormones, metabolism and body composition as major determinants of blood rheology: potential pathophysiological meaning.  Clin Hemorheol Microcirc . 2002;  26 63-79
    PubMedGoogle Scholar
  • 72 Mark M, Walter R, Harris L G, Reinhart W H. Influence of parathyroid hormone, calcitonin, 1,25(OH)2 cholecalciferol, calcium, and the calcium ionophore A23187 on erythrocyte morphology and blood viscosity.  J Lab Clin Med . 2000;  135 347-352
    CrossrefPubMedGoogle Scholar
  • 73 Baskurt O K, Levi E, Temizer A. et al . In vitro effects of thyroxine on the mechanical properties of erythrocytes.  Life Sci . 1990;  46 1471-1477
    CrossrefPubMedGoogle Scholar
  • 74 Cicco G, Carbonara M C, Stingi G D, Pirrelli A. Cytosolic calcium and hemorheological patterns during arterial hypertension.  Clin Hemorheol Microcirc . 2001;  24 25-31
    PubMedGoogle Scholar
  • 75 Kavanagh B D, Coffey B E, Needham D, Hochmuth R M, Dewhirst M W. The effect of flunarizine on erythrocyte suspension viscosity under conditions of extreme hypoxia, low pH, and lactate treatment.  Br J Cancer . 1993;  67 734-741
    PubMedGoogle Scholar
  • 76 Takakuwa Y, Ishibashi T, Mohandas N. Regulation of red cell membrane deformability and stability by skeletal protein network.  Biorheology . 1990;  27 357-365
    PubMedGoogle Scholar
  • 77 Takakuwa Y. Protein 4.1, a multifunctional protein of the erythrocyte membrane skeleton: structure and functions in erythrocytes and nonerythroid cells.  Int J Hematol . 2000;  72 298-309
    PubMedGoogle Scholar
  • 78 Friederichs E, Farley R A, Meiselman H J. Influence of calcium permeabilization and membrane-attached hemoglobin on erythrocyte deformability.  Am J Hematol . 1992;  41 170-177
    PubMedGoogle Scholar
  • 79 Baskurt O K. Activated granulocyte induced alterations in red blood cells and protection by antioxidant enzymes.  Clin Hemorheol . 1996;  16 49-56
    PubMedGoogle Scholar
  • 80 Yalcin O, Erman A, Muratl;di S, Bor-Küçükatay M, Başkurt O K. Time course of hemorheological alterations following heavy anaerobic exercise in untrained human subjects.  J Appl Physiol . 2003;  94 997-1002
    CrossrefPubMedGoogle Scholar
  • 81 Baskurt O K, Bor-Küçükatay M, Yalcin O, Meiselman H J. Aggregation behavior and electrophoretic mobility of red blood cells in various mammalian species.  Biorheology . 2000;  37 417-428
    PubMedGoogle Scholar
  • 82 Bor-Küçükatay M, Yalcin O, Meiselman H J, Baskurt O K. Erythropoietin-induced rheological changes of rat erythrocytes.  Br J Haematol . 2000;  110 82-88
    CrossrefPubMedGoogle Scholar
  • 83 Granger D N. Role of xanthine oxidase and granulocytes in ischemia reperfusion injury.  Am J Physiol . 1988;  255 H1269-H1275
    PubMedGoogle Scholar
  • 84 Welbourn C RB, Goldman G, Paterson I S. et al . Pathophysiology of ischaemia reperfusion injury: central role of the neutrophil.  Br J Surg . 1991;  78 651-655
    CrossrefPubMedGoogle Scholar
  • 85 Baskurt O K, Yavuzer S. Some hematological effects of oxidants. In: Nriagu JO, Simmons MS, eds. Environmental Oxidants New York: John Wiley 1994: 405-423
    Google Scholar
  • 86 Weiss S J. The role of superoxide in the destruction of erythrocyte targets by human neutrophils.  J Biol Chem . 1980;  255 9912-9917
    PubMedGoogle Scholar
  • 87 Snyder L M, Fortier N, Trainor J. et al . Effect of hydrogen peroxide exposure on normal human erythrocyte deformability, morphology, surface characteristics, and spectrin-hemoglobin cross-linking.  J Clin Invest . 1985;  76 1971-1977
    CrossrefPubMedGoogle Scholar
  • 88 Uyesaka N, Hasegawa S, Ishioka N. et al . Effect of superoxide anions on red cell deformability and membrane proteins.  Biorheology . 1992;  29 217-229
    PubMedGoogle Scholar
  • 89 Ali H, Haribabu B, Richardson R M, Snyderman R. Mechanisms of inflammation and leukocyte activation.  Med Clin North Am . 1997;  81 1-28
    CrossrefPubMedGoogle Scholar
  • 90 Downey G P, Fukushima T, Fialkow L, Waddell T K. Intracellular signaling in neutrophil priming and activation.  Semin Cell Biol . 1995;  6 345-356
    PubMedGoogle Scholar
  • 91 Claster S, Chiu D TY, Quintanilha A, Lubin B. Neutrophils mediate lipid peroxidation in human red cells.  Blood . 1984;  64 1079-1084
    PubMedGoogle Scholar
  • 92 Cokelet G R, Goldsmith H L. Decreased hydrodynamic resistance in the two-phase flow of blood through small vertical tubes at low flow rates.  Circ Res . 1991;  68 1-17
    CrossrefPubMedGoogle Scholar
  • 93 Fahraeus R. The influence of the rouleau formation of the erythrocytes on the rheology of the blood.  Acta Med Scand . 1958;  161 151-165
    PubMedGoogle Scholar
  • 94 McKay C B, Linderkamp O, Meiselman H J. Fahraeus and Fahraeus-Lindqvist effects for neonatal and adult RBC suspensions.  Pediatr Res . 1993;  34 538-543
    PubMedGoogle Scholar
  • 95 Murata T. Effects of sedimentation of small red blood cell aggregates on blood flow in narrow horizontal tubes.  Biorheology . 1996;  33 267-283
    CrossrefPubMedGoogle Scholar
  • 96 Reinke W, Gaehtgens P, Johnson P C. Blood viscosity in small tubes: effect of shear rate, aggregation and sedimentation.  Am J Physiol . 1987;  253 H540-H547
    PubMedGoogle Scholar
  • 97 Alonso C, Pries A R, Gaehtgens P. Time-dependent rheological behavior of blood at low shear in narrow vertical tubes.  Am J Physiol . 1993;  253 H553-H561
    PubMedGoogle Scholar
  • 98 McKay C B, Meiselman H J. Osmolality-mediated Fahraeus and Fahraeus-Lindqvist effects for human RBC suspensions.  Am J Physiol . 1988;  254 H238-H249
    PubMedGoogle Scholar
  • 99 Hakim T S. Eythrocyte deformability and segmental pulmonary vascular resistance: osmolarity and heat treatment.  J Appl Physiol . 1988;  65 1634-1641
    PubMedGoogle Scholar
  • 100 Parthasarathi K, Lipowsky H H. Capillary recruitment in response to tissue hypoxia and its dependence on red blood cell deformability.  Am J Physiol . 1999;  277 H2145-H2157
    PubMedGoogle Scholar
  • 101 Secomb T W, Hsu R. Resistance to blood flow in nonuniform capillaries.  Microcirculation . 1997;  4 421-427
    PubMedGoogle Scholar
  • 102 Schmid-Schönbein H. Fluid dynamics and hemorheology in vivo: the interactions of hemodynamic parameters and hemorheological "properties" in determining the flow behavior of blood in microvascular networks. In: Lowe GDO, ed. Clinical Blood Rheology Boca Raton, FL: CRC Press 1988: 129-219
    Google Scholar
  • 103 Klitzman B, Duling B R. Microvascular hematocrit and red cell flow in resting and contracting striated muscle.  Am J Physiol . 1979;  237 H481-H490
    PubMedGoogle Scholar
  • 104 Brizel D M, Klitzman B, Cook M. et al . A comparison of tumor and normal tissue microvascular hematocrits and red cell fluxes in a rat window chamber model.  Int J Radiat Oncol Biol Phys . 1993;  25 269-276
    PubMedGoogle Scholar
  • 105 Schmid-Schönbein G W, Zweifach B W. RBC velocity profiles in arterioles and venules of the rabbit omentum.  Microvasc Res . 1975;  10 153-164
    PubMedGoogle Scholar
  • 106 Lipowsky H H, Cram L E, Justice W, Eppihimer M J. Effect of erythrocyte deformability on in vivo red cell transit time and hematocrit and their correlation with in vitro filterability.  Microvasc Res . 1993;  46 43-64
    PubMedGoogle Scholar
  • 107 Baskurt O K, Edremitlioglu M, Temiz A. Effect of erythrocyte deformability on myocardial hematocrit gradient.  Am J Physiol . 1995;  37 H260-H264
    PubMedGoogle Scholar
  • 108 Baskurt O K, Edremitlioglu M. Myocardial tissue hematocrit: existence of a transmural gradient and alterations after fibrinogen infusions.  Clin Hemorheol . 1995;  15 97-105
    PubMedGoogle Scholar
  • 109 Suzuki Y, Tateishi N, Soutani M, Maeda N. Flow behavior of erythrocytes in microvessels and glass capillaries: effects of erythrocyte deformation and erythrocyte aggregation.  Int J Microcirc Clin Exp . 1996;  16 187-194
    PubMedGoogle Scholar
  • 110 Vicaut E. Opposite effects of red blood cell aggregation on resistance to blood flow.  J Cardiovasc Surg . 1995;  36 361-368
    PubMedGoogle Scholar
  • 111 Drussel J J, Berthault M F, Guiffant G, Dufaux J. Effects of red blood cell hyperaggregation on the rat microcirculation blood flow.  Acta Physiol Scand . 1998;  163 25-32
    CrossrefPubMedGoogle Scholar
  • 112 Mchedlishvili G, Gobejishvili L, Beritashvili N. Effect of intensified red blood cell aggregability on arterial pressure and mesenteric microcirculation.  Microvasc Res . 1993;  45 233-242
    PubMedGoogle Scholar
  • 113 Vicaut E, Hou X, Decuypere L, Taccoen A, Duvelleroy M. Red blood cell aggregation and microcirculation in rat cremaster muscle.  Int J Microcirc Clin Exp . 1994;  14 14-21
    PubMedGoogle Scholar
  • 114 Charansonney O, Mouren S, Dufaux S, Duvelleroy M, Vicaut E. Red blood cell aggregation and blood viscosity in an isolated heart preparation.  Biorheology . 1993;  30 75-84
    PubMedGoogle Scholar
  • 115 Rogausch H. The apparent viscosity of aggregating and non-aggregating erythrocyte suspensions in the isolated perfused liver.  Biorheology . 1987;  24 163-171
    PubMedGoogle Scholar
  • 116 Verkeste C M, Boekkooi P F, Saxena P R, Peeters L L. Increased red cell aggregation does not reduce uteroplacental blood flow in the awake, hemoconcentrated, late-pregnant guinea pig.  Pediatr Res . 1992;  31 91-93
    PubMedGoogle Scholar
  • 117 Cabel M, Meiselman H J, Popel A S, Johnson P C. Contribution of red cell aggregation to venous vascular resistance in skeletal muscle.  Am J Physiol . 1997;  272 H1020-H1032
    PubMedGoogle Scholar
  • 118 Baskurt O K, Bor-Küçükatay M, Yalcin O. The effect of red blood cell aggregation on blood flow resistance.  Biorheology . 1999;  36 447-452
    PubMedGoogle Scholar
  • 119 Calver A, Collier J, Vallace P. Nitric oxide and cardiovascular control.  Exp Physiol . 1993;  78 303-326
    PubMedGoogle Scholar
  • 120 Fleming I, Bauersachs J, Busse R. Calcium-dependent and calcium-independent activation of the endothelial NO synthase.  J Vasc Res . 1997;  34 165-174
    PubMedGoogle Scholar
  • 121 Vallance P, Chan N. Endothelial function and nitric oxide: clinical relevance.  Heart . 2001;  85 342-350
    CrossrefPubMedGoogle Scholar
  • 122 Nerem R M, Alexander R W, Chappell D C. et al . The study of the influence of flow on vascular endothelial biology.  Am J Med Sci . 1998;  316 169-175
    PubMedGoogle Scholar
      >