Transfusion Medicine Reviews
Volume 26, Issue 1 , Pages 1-13 , January 2012

Principles and Practice of Thromboelastography in Clinical Coagulation Management and Transfusion Practice

References 

  1. Hannon T. Trauma blood management: avoiding the collateral damage of trauma resuscitation protocols. Hematology. 2010;1:463–464
  2. Ferraris VA, Brown JR, Despotis GJ, et al. 2011 update to the society of thoracic surgeons and the society of cardiovascular anesthesiologists blood conservation clinical practice guidelines. Ann Thorac Surg. 2011;91:944–982
  3. Bolliger D, Gorlinger K, Tanaka KA. Pathophysiology and treatment of coagulopathy in massive hemorrhage and hemodilution. Anesthesiology. 2010;113:1205–1219
  4. Hartert H. Blutgerinnungsstudien mit der thromboelastographie, einem neuen Untersuchungsverfahren. Klin Wochenschrift. 1948;26:557–583
  5. White GC. The partial thromboplastin time: defining an era in coagulation. J Thromb Haemost. 2003;1:2267–2270
  6. Ganter MT, Hofer CK. Coagulation monitoring: current techniques and clinical use of viscoelastic point-of-care coagulation devices. Anesth Analg. 2008;106:1366–1375
  7. Jackson GN, Ashpole KJ, Yentis SM. The TEG vs the ROTEM thromboelastography/thromboelastometry systems. Anaesthesia. 2009;64:212–215
  8. Luddington RJ. Thromboelastography/thromboelastometry. Clin Lab Haematol. 2005;27:81–90
  9. Tomori T, Hupalo D, Teranishi K, et al. Evaluation of coagulation stages of hemorrhaged swine: comparison of thromboelastography and rotational elastometry. Blood Coagul Fibrinolysis. 2010;21:20–27
  10. Venema LF, Post WJ, Hendriks HG, Huet RC, de Wolf JT, de Vries AJ. An assessment of clinical interchangeability of TEG and ROTEM thromboelastographic variables in cardiac surgical patients. Anesth Analg. 2010;111:339–344
  11. Bolliger D, Szlam F, Molinaro RJ, Rahe-Meyer N, Levy JH, Tanaka KA. Finding the optimal concentration range for fibrinogen replacement after severe haemodilution: an in vitro model. Br J Anaesth. 2009;102:793–799
  12. Katori N, Szlam F, Levy JH, Tanaka KA. A novel method to assess platelet inhibition by eptifibatide with thrombelastograph. Anesth Analg. 2004;99:1794–1799
  13. Nielsen VG, Gurley WQ, Burch TM. The impact of factor XIII on coagulation kinetics and clot strength determined by thrombelastography. Anesth Analg. 2004;99:120–123
  14. Sorensen B, Ingerslev J. Whole blood clot formation phenotypes in hemophilia A and rare coagulation disorders. Patterns of response to recombinant factor VIIa. J Thromb Haemost. 2004;2:102–110
  15. Rivard GE, Brummel-Ziedins KE, Mann KG, Fan L, Hofer A, Cohen E. Evaluation of the profile of thrombin generation during the process of whole blood clotting as assessed by thrombelastography. J Thromb Haemost. 2005;3:2039–2043
  16. Schochl H, Nienaber U, Hofer G, et al. Goal-directed coagulation management of major trauma patients using thromboelastometry (ROTEM)–guided administration of fibrinogen concentrate and prothrombin complex concentrate. Crit Care. 2010;14:R55
  17. Chavez JJ, Foley DE, Snider CC, et al. A novel thrombelastograph tissue factor/kaolin assay of activated clotting times for monitoring heparin anticoagulation during cardiopulmonary bypass. Anesth Analg. 2004;99:1290–1294
  18. Noval-Padillo JA, Leon-Justel A, Mellado-Miras P, et al. Introduction of fibrinogen in the treatment of hemostatic disorders during orthotopic liver transplantation: implications in the use of allogenic blood. Transplant Proc. 2010;42:2973–2974
  19. Katori N, Tanaka KA, Szlam F, Levy JH. The effects of platelet count on clot retraction and tissue plasminogen activator-induced fibrinolysis on thrombelastography. Anesth Analg. 2005;100:1781–1785
  20. Wallin O, Soderberg J, Grankvist K, Jonsson PA, Hultdin J. Preanalytical effects of pneumatic tube transport on routine haematology, coagulation parameters, platelet function and global coagulation. Clin Chem Lab Med. 2008;46:1443–1449
  21. Coakley M, Reddy K, Mackie I, Mallett S. Transfusion triggers in orthotopic liver transplantation: a comparison of the thromboelastometry analyzer, the thromboelastogram, and conventional coagulation tests. J Cardiothorac Vasc Anesth. 2006;20:548–553
  22. Kang YG, Martin DJ, Marquez J, et al. Intraoperative changes in blood coagulation and thrombelastographic monitoring in liver transplantation. Anesth Analg. 1985;64:888–896
  23. Zambruni A, Thalheimer U, Leandro G, Perry D, Burroughs AK. Thromboelastography with citrated blood: comparability with native blood, stability of citrate storage and effect of repeated sampling. Blood Coagul Fibrinolysis. 2004;15:103–107
  24. Kashuk JL, Moore EE, Le T, et al. Noncitrated whole blood is optimal for evaluation of postinjury coagulopathy with point-of-care rapid thrombelastography. J Surg Res. 2009;156:133–138
  25. Sorensen B, Johansen P, Christiansen K, Woelke M, Ingerslev J. Whole blood coagulation thrombelastographic profiles employing minimal tissue factor activation. J Thromb Haemost. 2003;1:551–558
  26. Lang T, Bauters A, Braun SL, et al. Multi-centre investigation on reference ranges for ROTEM thromboelastometry. Blood Coagul Fibrinolysis. 2005;16:301–310
  27. Manufacturer's package insert. Boston (Mass): Haemonetics Corp.; 2010;
  28. Camenzind V, Bombeli T, Seifert B, et al. Citrate storage affects thrombelastograph analysis. Anesthesiology. 2000;92:1242–1249
  29. Rumph B, Bolliger D, Narang N, et al. In vitro comparative study of hemostatic components in warfarin-treated and fibrinogen-deficient plasma. J Cardiothorac Vasc Anesth. 2010;24:408–412
  30. MacDonald SG, Luddington RJ. Critical factors contributing to the thromboelastography trace. Semin Thromb Hemost. 2010;36:712–722
  31. Ferrucci L, Corsi A, Lauretani F, et al. The origins of age-related proinflammatory state. Blood. 2005;105:2294–2299
  32. Lang T, Johanning K, Metzler H, et al. The effects of fibrinogen levels on thromboelastometric variables in the presence of thrombocytopenia. Anesth Analg. 2009;108:751–758
  33. Rahe-Meyer N, Pichlmaier M, Haverich A, et al. Bleeding management with fibrinogen concentrate targeting a high-normal plasma fibrinogen level: a pilot study. Br J Anaesth. 2009;102:785–792
  34. Spiezia L, Radu C, Marchioro P, et al. Peculiar whole blood rotation thromboelastometry (Rotem) profile in 40 sideropenic anaemia patients. Thromb Haemost. 2008;100:1106–1110
  35. Oswald E, Stalzer B, Heitz E, et al. Thromboelastometry (ROTEM) in children: age-related reference ranges and correlations with standard coagulation tests. Br J Anaesth. 2010;105:827–835
  36. Strauss T, Levy-Shraga Y, Ravid B, et al. Clot formation of neonates tested by thromboelastography correlates with gestational age. Thromb Haemost. 2010;103:344–350
  37. Bolliger D, Szlam F, Suzuki N, Matsushita T, Tanaka KA. Heterozygous antithrombin deficiency improves in vivo haemostasis in factor VIII–deficient mice. Thromb Haemost. 2010;103:1233–1238
  38. Cvirn G, Gallistl S, Leschnik B, Muntean W. Low tissue factor pathway inhibitor (TFPI) together with low antithrombin allows sufficient thrombin generation in neonates. J Thromb Haemost. 2003;1:263–268
  39. Tantry US, Bliden KP, Gurbel PA. Overestimation of platelet aspirin resistance detection by thrombelastograph platelet mapping and validation by conventional aggregometry using arachidonic acid stimulation. J Am Coll Cardiol. 2005;46:1705–1709
  40. Craft RM, Chavez JJ, Bresee SJ, Wortham DC, Cohen E, Carroll RC. A novel modification of the thrombelastograph assay, isolating platelet function, correlates with optical platelet aggregation. J Lab Clin Med. 2004;143:301–309
  41. Scharbert G, Auer A, Kozek-Langenecker S. Evaluation of the Platelet Mapping Assay on rotational thromboelastometry ROTEM. Platelets. 2009;20:125–130
  42. Rahe-Meyer N, Solomon C, Vorweg M, et al. Multicentric comparison of single portion reagents and liquid reagents for thromboelastometry. Blood Coagul Fibrinolysis. 2009;20:218–222
  43. Solomon C, Cadamuro J, Ziegler B, et al. A comparison of fibrinogen measurement methods with fibrin clot elasticity assessed by thromboelastometry, before and after administration of fibrinogen concentrate in cardiac surgery patients. Transfusion. 2011;[epub ahead]
  44. Schochl H, Frietsch T, Pavelka M, Jambor C. Hyperfibrinolysis after major trauma: differential diagnosis of lysis patterns and prognostic value of thrombelastometry. J Trauma. 2009;67:125–131
  45. Rugeri L, Levrat A, David JS, et al. Diagnosis of early coagulation abnormalities in trauma patients by rotation thrombelastography. J Thromb Haemost. 2007;5:289–295
  46. Alexander DC, Butt WW, Best JD, Donath SM, Monagle PT, Shekerdemian LS. Correlation of thromboelastography with standard tests of anticoagulation in paediatric patients receiving extracorporeal life support. Thromb Res. 2010;125:387–392
  47. Young G, Ebbesen LS, Viuff D, et al. Evaluation of thromboelastography for monitoring recombinant activated factor VII ex vivo in haemophilia A and B patients with inhibitors: a multicentre trial. Blood Coagul Fibrinolysis. 2008;19:276–282
  48. Levi M, Levy JH, Andersen HF, Truloff D. Safety of recombinant activated factor VII in randomized clinical trials. N Engl J Med. 2010;363:1791–1800
  49. Keeney M, Allan DS, Lohmann RC, Yee IH. Effect of activated recombinant human factor 7 (Niastase) on laboratory testing of inhibitors of factors VIII and IX. Lab Hematol. 2005;11:118–123
  50. Viuff D, Andersen S, Sorensen BB, Lethagen S. Optimizing thrombelastography (TEG) assay conditions to monitor rFVIIa (NovoSeven) therapy in haemophilia A patients. Thromb Res. 2010;126:144–149
  51. Taketomi T, Szlam F, Vinten-Johansen J, Levy JH, Tanaka KA. Thrombin-activated thrombelastography for evaluation of thrombin interaction with thrombin inhibitors. Blood Coagul Fibrinolysis. 2007;18:761–767
  52. Brummel KE, Paradis SG, Butenas S, Mann KG. Thrombin functions during tissue factor–induced blood coagulation. Blood. 2002;100:148–152
  53. Bolliger D, Szlam F, Molinaro RJ, Escobar MA, Levy JH, Tanaka KA. Thrombin generation and fibrinolysis in anti-factor IX treated blood and plasma spiked with factor VIII inhibitor bypassing activity or recombinant factor VIIa. Haemophilia. 2010;16:510–517
  54. Taketomi T, Szlam F, Bader SO, Sheppard CA, Levy JH, Tanaka KA. Effects of recombinant activated factor VII on thrombin-mediated feedback activation of coagulation. Blood Coagul Fibrinolysis. 2008;19:135–141
  55. Butenas S, Brummel KE, Branda RF, Paradis SG, Mann KG. Mechanism of factor VIIa-dependent coagulation in hemophilia blood. Blood. 2002;99:923–930
  56. Lak M, Scharling B, Blemings A, et al. Evaluation of rFVIIa (NovoSeven) in Glanzmann patients with thromboelastogram. Haemophilia. 2008;14:103–110
  57. Nielsen VG, Cohen BM, Cohen E. Effects of coagulation factor deficiency on plasma coagulation kinetics determined via thrombelastography: critical roles of fibrinogen and factors II, VII, X and XII. Acta Anaesthesiol Scand. 2005;49:222–231
  58. Tanaka KA, Szlam F, Rusconi CP, Levy JH. In-vitro evaluation of anti-factor IXa aptamer on thrombin generation, clotting time, and viscoelastometry. Thromb Haemost. 2009;101:827–833
  59. Schneiderman J, Rubin E, Nugent DJ, Young G. Sequential therapy with activated prothrombin complex concentrates and recombinant FVIIa in patients with severe haemophilia and inhibitors: update of our previous experience. Haemophilia. 2007;13:244–248
  60. Bolliger D, Szlam F, Levy JH, Molinaro RJ, Tanaka KA. Haemodilution-induced profibrinolytic state is mitigated by fresh-frozen plasma: implications for early haemostatic intervention in massive haemorrhage. Br J Anaesth. 2010;104:318–325
  61. Hemker HC, Al Dieri R, De Smedt E, Beguin S. Thrombin generation, a function test of the haemostatic-thrombotic system. Thromb Haemost. 2006;96:553–561
  62. Lang T, Toller W, Gutl M, et al. Different effects of abciximab and cytochalasin D on clot strength in thrombelastography. J Thromb Haemost. 2004;2:147–153
  63. Zuckerman L, Cohen E, Vagher JP, Woodward E, Caprini JA. Comparison of thrombelastography with common coagulation tests. Thromb Haemost. 1981;46:752–756
  64. Orlikowski CE, Rocke DA, Murray WB, et al. Thrombelastography changes in pre-eclampsia and eclampsia. Br J Anaesth. 1996;77:157–161
  65. Larsen OH, Ingerslev J, Sorensen B. Whole blood laboratory model of thrombocytopenia for use in evaluation of hemostatic interventions. Ann Hematol. 2007;86:217–221
  66. Apelseth TO, Bruserud O, Wentzel-Larsen T, Hervig T. Therapeutic efficacy of platelet transfusion in patients with acute leukemia: an evaluation of methods. Transfusion. 2010;50:766–775
  67. Fressinaud E, Veyradier A, Truchaud F, et al. Screening for von Willebrand disease with a new analyzer using high shear stress: a study of 60 cases. Blood. 1998;91:1325–1331
  68. Fenger-Eriksen C, Moore GW, Rangarajan S, Ingerslev J, Sorensen B. Fibrinogen estimates are influenced by methods of measurement and hemodilution with colloid plasma expanders. Transfusion. 2010;50:2571–2576
  69. Hiippala ST. Dextran and hydroxyethyl starch interfere with fibrinogen assays. Blood Coagul Fibrinolysis. 1995;6:743–746
  70. Molinaro RJ, Szlam F, Levy JH, Fantz CR, Tanaka KA. Low plasma fibrinogen levels with the Clauss method during anticoagulation with bivalirudin. Anesthesiology. 2008;109:160–161
  71. Carroll RC, Craft RM, Chavez JJ, Snider CC, Kirby RK, Cohen E. Measurement of functional fibrinogen levels using the Thrombelastograph. J Clin Anesth. 2008;20:186–190
  72. Rahe-Meyer N, Solomon C, Winterhalter M, et al. Thromboelastometry-guided administration of fibrinogen concentrate for the treatment of excessive intraoperative bleeding in thoracoabdominal aortic aneurysm surgery. J Thorac Cardiovasc Surg. 2009;138:694–702
  73. Jambor C, Reul V, Schnider TW, Degiacomi P, Metzner H, Korte WC. In vitro inhibition of factor XIII retards clot formation, reduces clot firmness, and increases fibrinolytic effects in whole blood. Anesth Analg. 2009;109:1023–1028
  74. Emesis J. Regulation of the acute release of tissue-type plasminogen activator from the endothelium by coagulation activation products. Ann N Y Acad Scienc. 1992;667:249–258
  75. Levrat A, Gros A, Rugeri L, et al. Evaluation of rotation thrombelastography for the diagnosis of hyperfibrinolysis in trauma patients. Br J Anaesth. 2008;100:792–797
  76. Kashuk JL, Moore EE, Sawyer M, et al. Primary fibrinolysis is integral in the pathogenesis of the acute coagulopathy of trauma. Ann Surg. 2010;252:434–442
  77. Shakur H, Roberts I, Bautista R, et al. Effects of tranexamic acid on death, vascular occlusive events, and blood transfusion in trauma patients with significant haemorrhage (CRASH-2): a randomised, placebo-controlled trial. Lancet. 2010;376:23–32
  78. Brohi K, Cohen MJ, Ganter MT, et al. Acute coagulopathy of trauma: hypoperfusion induces systemic anticoagulation and hyperfibrinolysis. J Trauma. 2008;64:1211–1217
  79. Kawasaki J, Katori N, Kodaka M, Miyao H, Tanaka KA. Electron microscopic evaluations of clot morphology during thrombelastography. Anesth Analg. 2004;99:1440–1444
  80. Theusinger OM, Baulig W, Asmis LM, Seifert B, Spahn DR. In vitro factor XIII supplementation increases clot firmness in Rotation Thromboelastometry (ROTEM). Thromb Haemost. 2010;104:385–391
  81. Weber CF, Sanders JO, Friedrich K, et al. Role of thromboelastometry for the monitoring of factor XIII—a prospective observational study in neurosurgical patients. Hämostasiologie. 2011;31:111–117
  82. Aarts PA, van den Broek SA, Prins GW, Kuiken GD, Sixma JJ, Heethaar RM. Blood platelets are concentrated near the wall and red blood cells, in the center in flowing blood. Arteriosclerosis. 1988;8:819–824
  83. Slichter SJ. Relationship between platelet count and bleeding risk in thrombocytopenic patients. Transfus Med Rev. 2004;18:153–167
  84. Joist JH, Bauman JE, Sutera SP. Platelet adhesion and aggregation in pulsatile shear flow: effects of red blood cells. Thromb Res. 1998;92:S47–S52
  85. Ng KF, Lam CC, Chan LC. In vivo effect of haemodilution with saline on coagulation: a randomized controlled trial. Br J Anaesth. 2002;88:475–480
  86. Ruttmann TG, James MF, Viljoen JF. Haemodilution induces a hypercoagulable state. Br J Anaesth. 1996;76:412–414
  87. Ruttmann T. Hemodilution-induced hypercoagulability. Anesth Analg. 2003;96:1539
  88. Blajchman MA, Bordin JO, Bardossy L, Heddle NM. The contribution of the haematocrit to thrombocytopenic bleeding in experimental animals. Br J Haematol. 1994;86:347–350
  89. Cerutti E, Stratta C, Romagnoli R, et al. Thromboelastogram monitoring in the perioperative period of hepatectomy for adult living liver donation. Liver Transpl. 2004;10:289–294
  90. Dai Y, Lee A, Critchley LA, White PF. Does thromboelastography predict postoperative thromboembolic events? A systematic review of the literature. Anesth Analg. 2009;108:734–742
  91. Mahla E, Lang T, Vicenzi MN, et al. Thromboelastography for monitoring prolonged hypercoagulability after major abdominal surgery. Anesth Analg. 2001;92:572–577
  92. Sniecinski RM, Hursting MJ, Paidas MJ, Levy JH. Etiology and assessment of hypercoagulability with lessons from heparin-induced thrombocytopenia. Anesth Analg. 2011;112:46–58
  93. Bauer KA, Rosendaal FR, Heit JA. Hypercoagulability: too many tests, too much conflicting data. Hematology. 2002;1:353–368
  94. Lutsey PL, Folsom AR, Heckbert SR, Cushman M. Peak thrombin generation and subsequent venous thromboembolism: the Longitudinal Investigation of Thromboembolism Etiology (LITE) study. J Thromb Haemost. 2009;7:1639–1648
  95. Szlam F, Luan D, Bolliger D, et al. Anti-factor IXa Aptamer reduces propagation of thrombin generation in plasma anticoagulated with warfarin. Thromb Res. 2010;125:432–437
  96. Anderson L, Quasim I, Soutar R, Steven M, Macfie A, Korte W. An audit of red cell and blood product use after the institution of thromboelastometry in a cardiac intensive care unit. Transfus Med. 2006;16:31–39
  97. Shore-Lesserson L, Manspeizer HE, DePerio M, Francis S, Vela-Cantos F, Ergin MA. Thromboelastography-guided transfusion algorithm reduces transfusions in complex cardiac surgery. Anesth Analg. 1999;88:312–319
  98. Kashuk JL, Moore EE, Sawyer M, et al. Postinjury coagulopathy management: goal directed resuscitation via POC thrombelastography. Ann Surg. 2010;251:604–614
  99. Borgman MA, Spinella PC, Perkins JG, et al. The ratio of blood products transfused affects mortality in patients receiving massive transfusions at a combat support hospital. J Trauma. 2007;63:805–813
  100. Holcomb JB, Wade CE, Michalek JE, et al. Increased plasma and platelet to red blood cell ratios improves outcome in 466 massively transfused civilian trauma patients. Ann Surg. 2008;248:447–458
  101. Watson GA, Sperry JL, Rosengart MR, et al. Fresh frozen plasma is independently associated with a higher risk of multiple organ failure and acute respiratory distress syndrome. J Trauma. 2009;67:221–227
  102. Nuttall GA, Oliver WC, Santrach PJ, et al. Efficacy of a simple intraoperative transfusion algorithm for nonerythrocyte component utilization after cardiopulmonary bypass. Anesthesiology. 2001;94:773–781
  103. Steiner ME, Despotis GJ. Transfusion algorithms and how they apply to blood conservation: the high-risk cardiac surgical patient. Hematol Oncol Clin North Am. 2007;21:177–184
  104. Afshari A, Wikkelso A, Brok J, Moller AM, Wetterslev J. Thrombelastography (TEG) or thromboelastometry (ROTEM) to monitor haemotherapy versus usual care in patients with massive transfusion. Cochrane Database Syst Rev. 2011;3:CD007871
  105. Hiippala ST, Myllyla GJ, Vahtera EM. Hemostatic factors and replacement of major blood loss with plasma-poor red cell concentrates. Anesth Analg. 1995;81:360–365
  106. Manco-Johnson MJ, Dimichele D, Castaman G, et al. Pharmacokinetics and safety of fibrinogen concentrate. J Thromb Haemost. 2009;7:2064–2069

 Conflicts of interest: DB received honoraria for lecturing from TEM International, Munich, Germany. KAT served on the advisory board for TEM International, Munich, Germany.

PII: S0887-7963(11)00064-2

doi: 10.1016/j.tmrv.2011.07.005

Transfusion Medicine Reviews
Volume 26, Issue 1 , Pages 1-13 , January 2012