Thrombotic Risks in Red Blood Cell Transfusions

Seminars in Thrombosis and Hemostasis

Volumn 42, Issue 2, 2016, Pages 102-111

  Dubovoy, Timur ^a   Engoren, Milo ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

erythrocytes; hemorrhage; thrombosis; transfusion

Indexed keywords

ADENOSINE TRIPHOSPHATE; BLOOD CLOTTING FACTOR 10A; CALCIUM; HEMOGLOBIN; NITRIC OXIDE; PHOSPHOLIPID; THROMBIN;

ARTERIAL THROMBOEMBOLISM; ARTICLE; BLEEDING; BLOOD GROUP ABO SYSTEM; BLOOD VISCOSITY; ENDOTHELIAL MICROPARTICLE; ERYTHROCYTE ADHESIVENESS; ERYTHROCYTE AGGREGATION; ERYTHROCYTE DEFORMABILITY; ERYTHROCYTE PRESERVATION; ERYTHROCYTE SHAPE; ERYTHROCYTE TRANSFUSION; HEART INFARCTION; HEMATOCRIT; HEMOSTASIS; HUMAN; META ANALYSIS (TOPIC); PATHOGENESIS; PRIORITY JOURNAL; SHEAR RATE; SICKLE CELL ANEMIA; SUBARACHNOID HEMORRHAGE; SYSTEMATIC REVIEW (TOPIC); THROMBOCYTE AGGREGATION; THROMBOSIS; UPPER GASTROINTESTINAL BLEEDING; VASCULAR ENDOTHELIUM; VENOUS THROMBOEMBOLISM; ADVERSE EFFECTS; BLOOD; CELL ADHESION; ERYTHROCYTE; HEMORRHAGE; METABOLISM; PATHOLOGY; RISK FACTOR; SIGNAL TRANSDUCTION;

CELL ADHESION; ENDOTHELIUM, VASCULAR; ERYTHROCYTE TRANSFUSION; ERYTHROCYTES; HEMORRHAGE; HUMANS; NITRIC OXIDE; RISK FACTORS; SIGNAL TRANSDUCTION; THROMBOSIS;

EID: 84959175772     PISSN: 00946176     EISSN: 10989064     Source Type: Journal    
DOI: 10.1055/s-0035-1569069     Document Type: Article

References (110)

1. Small M., Lowe G. D., Cameron E., Forbes C. D. Contribution of the haematocrit to the bleeding time. Haemostasis: 1983; 13 6 379 384
2. Soltani G., Fernandez F., Pris J., Boneu B. Prolonged bleeding time in severe anemia [in French]. Presse Med: 1986; 15 16 745 747
3. Tokish J. M., Kocher M. S., Hawkins R. J. Ergogenic aids: a review of basic science, performance, side effects, and status in sports. Am J Sports Med: 2004; 32 6 1543 1553
4. Andrews D. A., Low P. S. Role of red blood cells in thrombosis. Curr Opin Hematol: 1999; 6 2 76 82
5. Mehrabadi M., Ku D. N., Aidun C. K. A continuum model for platelet transport in flowing blood based on direct numerical simulations of cellular blood flow. Ann Biomed Eng: 2015; 43 6 1410 1421
6. Vahidkhah K., Diamond S. L., Bagchi P. Platelet dynamics in three-dimensional simulation of whole blood. Biophys J: 2014; 106 11 2529 2540
7. Greenwalt T. J. The how and why of exocytic vesicles. Transfusion: 2006; 46 1 143 152
8. Beusterien K. M., Nissenson A. R., Port F. K., Kelly M., Steinwald B., Ware J. E. Jr. The effects of recombinant human erythropoietin on functional health and well-being in chronic dialysis patients. J Am Soc Nephrol: 1996; 7 5 763 773
9. Hébert P. C., Wells G., Blajchman M. A., et al. A multicenter, randomized, controlled clinical trial of transfusion requirements in critical care. Transfusion Requirements in Critical Care Investigators, Canadian Critical Care Trials Group. N Engl J Med: 1999; 340 6 409 417
10. Baskurt O. K., Meiselman H. J. Iatrogenic hyperviscosity and thrombosis. Semin Thromb Hemost: 2012; 38 8 854 864
11. Chien S. Red cell deformability and its relevance to blood flow. Annu Rev Physiol: 1987; 49 177 192
12. Cosemans J. M., Angelillo-Scherrer A., Mattheij N. J., Heemskerk J. W. The effects of arterial flow on platelet activation, thrombus growth, and stabilization. Cardiovasc Res: 2013; 99 2 342 352
13. Grabowski E. F., Yam K., Gerace M. Evaluation of hemostasis in flowing blood. Am J Hematol: 2012; 87 01 S51 S55
14. De Franceschi L., Cappellini M. D., Olivieri O. Thrombosis and sickle cell disease. Semin Thromb Hemost: 2011; 37 3 226 236
15. Steinberg M. H. Management of sickle cell disease. N Engl J Med: 1999; 340 13 1021 1030
16. Colin Y., Le Van Kim C., El Nemer W. Red cell adhesion in human diseases. Curr Opin Hematol: 2014; 21 3 186 192
17. Wandersee N. J., Olson S. C., Holzhauer S. L., Hoffmann R. G., Barker J. E., Hillery C. A. Increased erythrocyte adhesion in mice and humans with hereditary spherocytosis and hereditary elliptocytosis. Blood: 2004; 103 2 710 716
18. Anand A., Feffer S. E. Hematocrit and bleeding time: an update. South Med J: 1994; 87 3 299 301
19. Duke W. W. The relation of blood platelets to hemorrhagic disease. By W.W. Duke. JAMA: 1983; 250 9 1201 1209
20. Hellem A. J., Borchgrevink C. F., Ames S. B. The role of red cells in haemostasis: the relation between haematocrit, bleeding time and platelet adhesiveness. Br J Haematol: 1961; 7 42 50
21. Livio M., Gotti E., Marchesi D., Mecca G., Remuzzi G., de Gaetano G. Uraemic bleeding: role of anaemia and beneficial effect of red cell transfusions. Lancet: 1982; 2 8306 1013 1015
22. Aarts P. A., van den Broek S. A., Prins G. W., Kuiken G. D., Sixma J. J., Heethaar R. M. Blood platelets are concentrated near the wall and red blood cells, in the center in flowing blood. Arteriosclerosis: 1988; 8 6 819 824
23. Baumgartner H. R. The role of blood flow in platelet adhesion, fibrin deposition, and formation of mural thrombi. Microvasc Res: 1973; 5 2 167 179
24. Dosne A. M., Merville C., Drouet L., Antonini G., Guiffant G., Quemada D. Importance of transport mechanisms in circulating blood for platelet deposition on arterial subendothelium. Microvasc Res: 1977; 14 1 45 52
25. Turitto V. T., Baumgartner H. R. Platelet interaction with subendothelium in a perfusion system: physical role of red blood cells. Microvasc Res: 1975; 9 3 335 344
26. Chen H., Angerer J. I., Napoleone M., et al. Hematocrit and flow rate regulate the adhesion of platelets to von Willebrand factor. Biomicrofluidics: 2013; 7 6 64113
27. Turitto V. T., Weiss H. J. Red blood cells: their dual role in thrombus formation. Science: 1980; 207 4430 541 543
28. Marchioli R., Finazzi G., Landolfi R., et al. Vascular and neoplastic risk in a large cohort of patients with polycythemia vera. J Clin Oncol: 2005; 23 10 2224 2232
29. Begg T. B., Hearns J. B. Components in blood viscosity. The relative contribution of haematocrit, plasma fibrinogen and other proteins. Clin Sci: 1966; 31 1 87 93
30. Kwaan H. C., Wang J. Hyperviscosity in polycythemia vera and other red cell abnormalities. Semin Thromb Hemost: 2003; 29 5 451 458
31. Pearson T. C., Wetherley-Mein G. Vascular occlusive episodes and venous haematocrit in primary proliferative polycythaemia. Lancet: 1978; 2 8102 1219 1222
32. El Nemer W., De Grandis M., Brusson M. Abnormal adhesion of red blood cells in polycythemia vera: a prothrombotic effect? Thromb Res: 2014; 133 02 S107 S111
33. Baxter E. J., Scott L. M., Campbell P. J., et al. Cancer Genome Project. Acquired mutation of the tyrosine kinase JAK2 in human myeloproliferative disorders. Lancet: 2005; 365 9464 1054 1061
34. James C., Ugo V., Le Couédic J. P., et al. A unique clonal JAK2 mutation leading to constitutive signalling causes polycythaemia vera. Nature: 2005; 434 7037 1144 1148
35. Kralovics R., Passamonti F., Buser A. S., et al. A gain-of-function mutation of JAK2 in myeloproliferative disorders. N Engl J Med: 2005; 352 17 1779 1790
36. Lippert E., Boissinot M., Kralovics R., et al. The JAK2-V617F mutation is frequently present at diagnosis in patients with essential thrombocythemia and polycythemia vera. Blood: 2006; 108 6 1865 1867
37. Wautier M. P., El Nemer W., Gane P., et al. Increased adhesion to endothelial cells of erythrocytes from patients with polycythemia vera is mediated by laminin alpha5 chain and Lu/BCAM. Blood: 2007; 110 3 894 901
38. Lubarsky D. A., Gallagher C. J., Berend J. L. Secondary polycythemia does not increase the risk of perioperative hemorrhagic or thrombotic complications. J Clin Anesth: 1991; 3 2 99 103
39. Nadeem O., Gui J., Ornstein D. L. Prevalence of venous thromboembolism in patients with secondary polycythemia. Clin Appl Thromb Hemost: 2013; 19 4 363 366
40. Schwarcz T. H., Hogan L. A., Endean E. D., Roitman I. T., Kazmers A., Hyde G. L. Thromboembolic complications of polycythemia: polycythemia vera versus smokers' polycythemia. J Vasc Surg: 1993; 17 3 518 522, discussion 522-523
41. Barr J. D., Chauhan A. K., Schaeffer G. V., Hansen J. K., Motto D. G. Red blood cells mediate the onset of thrombosis in the ferric chloride murine model. Blood: 2013; 121 18 3733 3741
42. Zhou S., Welsby I. Is ABO blood group truly a risk factor for thrombosis and adverse outcomes? World J Cardiol: 2014; 6 9 985 992
43. Dick W., Schneider W., Brockmueller K., Mayer W. Interrelations of Thrombo-Embolic Diseases and Blood-Group Distribution. Thromb Diath Haemorrh: 1963; 143 472 474
44. Jick H., Slone D., Westerholm B., et al. Venous thromboembolic disease and ABO blood type. A cooperative study. Lancet: 1969; 1 7594 539 542
45. Robinson W. M., Roisenberg I. Venous thromboembolism and ABO blood groups in a Brazilian population. Hum Genet: 1980; 55 1 129 131
46. Wautrecht J. C., Galle C., Motte S., Dereume J. P., Dramaix M. The role of ABO blood groups in the incidence of deep vein thrombosis. Thromb Haemost: 1998; 79 3 688 689
47. Gill J. C., Endres-Brooks J., Bauer P. J., Marks W. J. Jr, Montgomery R. R. The effect of ABO blood group on the diagnosis of von Willebrand disease. Blood: 1987; 69 6 1691 1695
48. Liumbruno G. M., Franchini M. Hemostasis, cancer, and ABO blood group: the most recent evidence of association. J Thromb Thrombolysis: 2014; 38 2 160 166
49. Moeller A., Weippert-Kretschmer M., Prinz H., Kretschmer V. Influence of ABO blood groups on primary hemostasis. Transfusion: 2001; 41 1 56 60
50. Kyrle P. A., Minar E., Hirschl M., et al. High plasma levels of factor VIII and the risk of recurrent venous thromboembolism. N Engl J Med: 2000; 343 7 457 462
51. Jenkins P. V., O'Donnell J. S. ABO blood group determines plasma von Willebrand factor levels: a biologic function after all? Transfusion: 2006; 46 10 1836 1844
52. Ruggeri Z. M., Zimmerman T. S. The complex multimeric composition of factor VIII/von Willebrand factor. Blood: 1981; 57 6 1140 1143
53. Nichols W. C., Ginsburg D. von Willebrand disease. Medicine (Baltimore): 1997; 76 1 1 20
54. Zheng X. L. ADAMTS13, TTP and Beyond. Hereditary Genet: 2013; 2 1 e104
55. Wu O., Bayoumi N., Vickers M. A., Clark P. ABO(H) blood groups and vascular disease: a systematic review and meta-analysis. J Thromb Haemost: 2008; 6 1 62 69
56. Dentali F., Sironi A. P., Ageno W., et al. Non-O blood type is the commonest genetic risk factor for VTE: results from a meta-analysis of the literature. Semin Thromb Hemost: 2012; 38 5 535 548
57. He M., Wolpin B., Rexrode K., et al. ABO blood group and risk of coronary heart disease in two prospective cohort studies. Arterioscler Thromb Vasc Biol: 2012; 32 9 2314 2320
58. Reilly M. P., Li M., He J., et al. Myocardial Infarction Genetics Consortium; Wellcome Trust Case Control Consortium. Identification of ADAMTS7 as a novel locus for coronary atherosclerosis and association of ABO with myocardial infarction in the presence of coronary atherosclerosis: two genome-wide association studies. Lancet: 2011; 377 9763 383 392
59. Koch C. G., Li L., Sessler D. I., et al. Duration of red-cell storage and complications after cardiac surgery. N Engl J Med: 2008; 358 12 1229 1239
60. Piccin A., Murphy W. G., Smith O. P. Circulating microparticles: pathophysiology and clinical implications. Blood Rev: 2007; 21 3 157 171
61. Rubin O., Canellini G., Delobel J., Lion N., Tissot J. D. Red blood cell microparticles: clinical relevance. Transfus Med Hemother: 2012; 39 5 342 347
62. Rubin O., Crettaz D., Tissot J. D., Lion N. Microparticles in stored red blood cells: submicron clotting bombs? Blood Transfus: 2010; 8 03 s31 s38
63. Zwaal R. F., Comfurius P., Bevers E. M. Scott syndrome, a bleeding disorder caused by defective scrambling of membrane phospholipids. Biochim Biophys Acta: 2004; 1636 2-3 119 128
64. Willekens F. L., Werre J. M., Groenen-Döpp Y. A., Roerdinkholder-Stoelwinder B., de Pauw B., Bosman G. J. Erythrocyte vesiculation: a self-protective mechanism? Br J Haematol: 2008; 141 4 549 556
65. Willekens F. L., Werre J. M., Kruijt J. K., et al. Liver Kupffer cells rapidly remove red blood cell-derived vesicles from the circulation by scavenger receptors. Blood: 2005; 105 5 2141 2145
66. van Beers E. J., Schaap M. C., Berckmans R. J., et al. CURAMA study group. Circulating erythrocyte-derived microparticles are associated with coagulation activation in sickle cell disease. Haematologica: 2009; 94 11 1513 1519
67. Mertens K., Bertina R. M. The contribution of Ca2+ and phospholipids to the activation of human blood-coagulation Factor X by activated Factor IX. Biochem J: 1984; 223 3 607 615
68. Sinauridze E. I., Kireev D. A., Popenko N. Y., et al. Platelet microparticle membranes have 50- to 100-fold higher specific procoagulant activity than activated platelets. Thromb Haemost: 2007; 97 3 425 434
69. Chung S. M., Bae O. N., Lim K. M., et al. Lysophosphatidic acid induces thrombogenic activity through phosphatidylserine exposure and procoagulant microvesicle generation in human erythrocytes. Arterioscler Thromb Vasc Biol: 2007; 27 2 414 421
70. Beleznay Z., Zachowski A., Devaux P. F., Navazo M. P., Ott P. ATP-dependent aminophospholipid translocation in erythrocyte vesicles: stoichiometry of transport. Biochemistry: 1993; 32 12 3146 3152
71. Zwaal R. F., Bevers E. M., Comfurius P., Rosing J., Tilly R. H., Verhallen P. F. Loss of membrane phospholipid asymmetry during activation of blood platelets and sickled red cells; mechanisms and physiological significance. Mol Cell Biochem: 1989; 91 1-2 23 31
72. Bevers E. M., Wiedmer T., Comfurius P., et al. Defective Ca(2+)-induced microvesiculation and deficient expression of procoagulant activity in erythrocytes from a patient with a bleeding disorder: a study of the red blood cells of Scott syndrome. Blood: 1992; 79 2 380 388
73. Biró E., Sturk-Maquelin K. N., Vogel G. M., et al. Human cell-derived microparticles promote thrombus formation in vivo in a tissue factor-dependent manner. J Thromb Haemost: 2003; 1 12 2561 2568
74. Doyle M. P., Hoekstra J. W. Oxidation of nitrogen oxides by bound dioxygen in hemoproteins. J Inorg Biochem: 1981; 14 4 351 358
75. Gladwin M. T., Lancaster J. R. Jr, Freeman B. A., Schechter A. N. Nitric oxide's reactions with hemoglobin: a view through the SNO-storm. Nat Med: 2003; 9 5 496 500
76. Allen B. W., Stamler J. S., Piantadosi C. A. Hemoglobin, nitric oxide and molecular mechanisms of hypoxic vasodilation. Trends Mol Med: 2009; 15 10 452 460
77. Jia L., Bonaventura C., Bonaventura J., Stamler J. S. S-nitrosohaemoglobin: a dynamic activity of blood involved in vascular control. Nature: 1996; 380 6571 221 226
78. Pawloski J. R., Swaminathan R. V., Stamler J. S. Cell-free and erythrocytic S-nitrosohemoglobin inhibits human platelet aggregation. Circulation: 1998; 97 3 263 267
79. Simon D. I., Stamler J. S., Jaraki O., et al. Antiplatelet properties of protein S-nitrosothiols derived from nitric oxide and endothelium-derived relaxing factor. Arterioscler Thromb: 1993; 13 6 791 799
80. Chin-Yee I., Arya N., d'Almeida M. S. The red cell storage lesion and its implication for transfusion. Transfus Sci: 1997; 18 3 447 458
81. Bosman G. J., Werre J. M., Willekens F. L., Novotný V. M. Erythrocyte ageing in vivo and in vitro: structural aspects and implications for transfusion. Transfus Med: 2008; 18 6 335 347
82. Lion N., Crettaz D., Rubin O., Tissot J. D. Stored red blood cells: a changing universe waiting for its map(s). J Proteomics: 2010; 73 3 374 385
83. Bennett-Guerrero E., Veldman T. H., Doctor A., et al. Evolution of adverse changes in stored RBCs. Proc Natl Acad Sci U S A: 2007; 104 43 17063 17068
84. Gao Y., Lv L., Liu S., Ma G., Su Y. Elevated levels of thrombin-generating microparticles in stored red blood cells. Vox Sang: 2013; 105 1 11 17
85. Rubin O., Crettaz D., Canellini G., Tissot J. D., Lion N. Microparticles in stored red blood cells: an approach using flow cytometry and proteomic tools. Vox Sang: 2008; 95 4 288 297
86. Donadee C., Raat N. J., Kanias T., et al. Nitric oxide scavenging by red blood cell microparticles and cell-free hemoglobin as a mechanism for the red cell storage lesion. Circulation: 2011; 124 4 465 476
87. Riccio D. A., Zhu H., Foster M. W., et al. Renitrosylation of banked human red blood cells improves deformability and reduces adhesivity. Transfusion: 2015
88. Keating F. K., Butenas S., Fung M. K., Schneider D. J. Platelet-white blood cell (WBC) interaction, WBC apoptosis, and procoagulant activity in stored red blood cells. Transfusion: 2011; 51 5 1086 1095
89. Carpeggiani C., Coceani M., Landi P., Michelassi C., L'abbate A. ABO blood group alleles: A risk factor for coronary artery disease. An angiographic study. Atherosclerosis: 2010; 211 2 461 466
90. Wiggins K. L., Smith N. L., Glazer N. L., et al. ABO genotype and risk of thrombotic events and hemorrhagic stroke. J Thromb Haemost: 2009; 7 2 263 269
91. Roeloffzen W. W., Kluin-Nelemans H. C., Bosman L., de Wolf J. T. Effects of red blood cells on hemostasis. Transfusion: 2010; 50 7 1536 1544
92. Larsen A. M., Leinoe E. B., Johansson P. I., Birgens H., Ostrowski S. R. Haemostatic function and biomarkers of endothelial damage before and after RBC transfusion in patients with haematologic disease. Vox Sang: 2015; 109 1 52 61
93. Silvain J., Pena A., Cayla G., et al. Impact of red blood cell transfusion on platelet activation and aggregation in healthy volunteers: results of the TRANSFUSION study. Eur Heart J: 2010; 31 22 2816 2821
94. Silvain J., Abtan J., Kerneis M., et al. Impact of red blood cell transfusion on platelet aggregation and inflammatory response in anemic coronary and noncoronary patients: the TRANSFUSION-2 study (impact of transfusion of red blood cell on platelet activation and aggregation studied with flow cytometry use and light transmission aggregometry). J Am Coll Cardiol: 2014; 63 13 1289 1296
95. Blair S. D., Janvrin S. B., McCollum C. N., Greenhalgh R. M. Effect of early blood transfusion on gastrointestinal haemorrhage. Br J Surg: 1986; 73 10 783 785
96. Restellini S., Kherad O., Jairath V., Martel M., Barkun A. N. Red blood cell transfusion is associated with increased rebleeding in patients with nonvariceal upper gastrointestinal bleeding. Aliment Pharmacol Ther: 2013; 37 3 316 322
97. Villanueva C., Colomo A., Bosch A., et al. Transfusion strategies for acute upper gastrointestinal bleeding. N Engl J Med: 2013; 368 1 11 21
98. Thai L., McCarn K., Stott W., et al. Venous thromboembolism in patients with head and neck cancer after surgery. Head Neck: 2013; 35 1 4 9
99. Lee H. K., Kim D. H., Jin U. S., Jeon Y. T., Hwang J. W., Park H. P. Effect of perioperative transfusion of old red blood cells on postoperative complications after free muscle sparing transverse rectus abdominis myocutaneous flap surgery for breast reconstruction. Microsurgery: 2014; 34 6 434 438
100. Khorana A. A., Francis C. W., Blumberg N., Culakova E., Refaai M. A., Lyman G. H. Blood transfusions, thrombosis, and mortality in hospitalized patients with cancer. Arch Intern Med: 2008; 168 21 2377 2381
101. Xenos E. S., Vargas H. D., Davenport D. L. Association of blood transfusion and venous thromboembolism after colorectal cancer resection. Thromb Res: 2012; 129 5 568 572
102. Kumar M. A., Boland T. A., Baiou M., et al. Red blood cell transfusion increases the risk of thrombotic events in patients with subarachnoid hemorrhage. Neurocrit Care: 2014; 20 1 84 90
103. Tan T. W., Farber A., Hamburg N. M., et al. Vascular Study Group of New England. Blood transfusion for lower extremity bypass is associated with increased wound infection and graft thrombosis. J Am Coll Surg: 2013; 216 5 1005 1014.e2, quiz 1031-1033
104. Paone G., Likosky D. S., Brewer R., et al. Membership of the Michigan Society of Thoracic and Cardiovascular Surgeons. Transfusion of 1 and 2 units of red blood cells is associated with increased morbidity and mortality. Ann Thorac Surg: 2014; 97 1 87 93, discussion 93-94
105. Schwann T. A., Kistler L., Engoren M. C., Habib R. H. Incidence and predictors of postoperative deep vein thrombosis in cardiac surgery in the era of aggressive thromboprophylaxis. Ann Thorac Surg: 2010; 90 3 760 766, discussion 766-768
106. Engoren M., Schwann T. A., Jewell E., et al. Is transfusion associated with graft occlusion after cardiac operations? Ann Thorac Surg: 2015; 99 2 502 508
107. Rao S. V., Jollis J. G., Harrington R. A., et al. Relationship of blood transfusion and clinical outcomes in patients with acute coronary syndromes. JAMA: 2004; 292 13 1555 1562
108. Carson J. L., Grossman B. J., Kleinman S., et al. Clinical Transfusion Medicine Committee of the AABB. Red blood cell transfusion: a clinical practice guideline from the AABB∗. Ann Intern Med: 2012; 157 1 49 58
109. Adams R. J., McKie V. C., Hsu L., et al. Prevention of a first stroke by transfusions in children with sickle cell anemia and abnormal results on transcranial Doppler ultrasonography. N Engl J Med: 1998; 339 1 5 11
110. DeBaun M. R., Gordon M., McKinstry R. C., et al. Controlled trial of transfusions for silent cerebral infarcts in sickle cell anemia. N Engl J Med: 2014; 371 8 699 710