Fibrinolysis in Trauma: “Myth,” “Reality,” or “Something in Between”

Seminars in Thrombosis and Hemostasis

Volumn 43, Issue 2, 2017, Pages 200-212

  Walsh, Mark ^a   Shreve, Jacob ^a   Thomas, Scott ^a   Moore, Ernest ^b   Moore, Hunter ^b   Hake, Daniel ^a   Pohlman, Tim ^a   Davis, Patrick ^a,c   Ploplis, Victoria ^d   Piscoya, Andres ^a,e   Wegner, Julie ^f   Bryant, John ^a   Crepinsek, Anton ^a   Lantry, James ^g   Sheppard, Forest ^h   Castellino, Francis ^d  

^a is an assistant professor of nursing at Bethel College   (United States)

^b DENVER HEALTH MEDICAL CENTER   (United States)

^c EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d UNIVERSITY OF NOTRE DAME   (United States)

^e WALTER REED ARMY MEDICAL CENTER   (United States)

^f MIDWESTERN UNIVERSITY   (United States)

^g San Antonio Military Medicine Center SAUSHEC   (United States)

^h Naval Medical Research Unit   (United States)

Author keywords

activated protein C; fibrinolysis; fibrinolytic shutdown; fibrinolytic spectrum; hemorrhagic phenotype; hyperfibrinolysis; rotational thromboelastometry; thromboelastography; tissue injury phenotype; tranexamic acid; trauma induced coagulopathy

Indexed keywords

BLOOD CLOTTING FACTOR; FIBRINOGEN; TRANEXAMIC ACID;

ARTICLE; BLOOD; BLOOD CLOTTING; BLOOD CLOTTING DISORDER; DISSEMINATED INTRAVASCULAR CLOTTING; ENDOTHELIUM; FIBRINOLYSIS; GLYCOCALYX; HEMOSTASIS; HYPOTHESIS; INJURY; PLASMA; PRIORITY JOURNAL; THEORY; THROMBOELASTOGRAPHY; VISCOELASTICITY; HUMAN; PHYSIOLOGY;

FIBRINOLYSIS; HUMANS; WOUNDS AND INJURIES;

EID: 85013453465     PISSN: 00946176     EISSN: 10989064     Source Type: Journal    
DOI: 10.1055/s-0036-1597900     Document Type: Article

References (123)

1. Ratnoff O D Some relationships among hemostasis, fibrinolytic phenomena, immunity, and the inflammatory response Adv Immunol 1969 10 145 227
2. Fourrier F Severe sepsis, coagulation, and fibrinolysis: dead end or one way? Crit Care Med 2012 40 9 2704 2708
3. Gando S Acute coagulopathy of trauma shock and coagulopathy of trauma: a rebuttal. You are now going down the wrong path J Trauma 2009 67 2 381 383
4. Brohi K Cohen M J Ganter M T Matthay M A Mackersie R C Pittet J F Acute traumatic coagulopathy: initiated by hypoperfusion: modulated through the protein C pathway? Ann Surg 2007 245 5 812 818
5. Brohi K Singh J Heron M Coats T Acute traumatic coagulopathy J Trauma 2003 54 6 1127 1130
6. Shakur H Roberts I Bautista R, et al; CRASH-2 trial collaborators. 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 (9734): 23 32
7. Napolitano L M Cohen M J Cotton B A Schreiber M A Moore E E Tranexamic acid in trauma: how should we use it? J Trauma Acute Care Surg 2013 74 6 1575 1586
8. Cap A Hunt B J The pathogenesis of traumatic coagulopathy Anaesthesia 2015 70 01 96 101, e32-e34
9. Campbell J E Aden J K Cap A P Acute traumatic coagulopathy: Whole blood thrombelastography measures the tip of the iceberg J Trauma Acute Care Surg 2015 78 5 955 961
10. Campbell J E Meledeo M A Cap A P Comparative response of platelet fV and plasma fV to activated protein C and relevance to a model of acute traumatic coagulopathy PLoS One 2014 9 6 e99181
11. Harvin J A Peirce C A Mims M M, et al. The impact of tranexamic acid on mortality in injured patients with hyperfibrinolysis J Trauma Acute Care Surg 2015 78 5 905 909, discussion 909-911
12. Valle E J Allen C J Van Haren R M, et al. Do all trauma patients benefit from tranexamic acid? J Trauma Acute Care Surg 2014 76 6 1373 1378
13. Cotton B A Harvin J A Kostousouv V, et al. Hyperfibrinolysis at admission is an uncommon but highly lethal event associated with shock and prehospital fluid administration J Trauma Acute Care Surg 2012 73 2 365 370, discussion 370
14. Gando S Hayakawa M Pathophysiology of trauma-Induced coagulopathy and management of critical bleeding requiring massive transfusion Semin Thromb Hemost 2016 42 2 155 165
15. Hess J R Brohi K Dutton R P, et al. The coagulopathy of trauma: a review of mechanisms J Trauma 2008 65 4 748 754
16. Gando S Wada H Thachil J; Scientific and Standardization Committee on DIC of the International Society on Thrombosis and Haemostasis (ISTH). Differentiating disseminated intravascular coagulation (DIC) with the fibrinolytic phenotype from coagulopathy of trauma and acute coagulopathy of trauma-shock (COT/ACOTS) J Thromb Haemost 2013 11 5 826 835
17. Chang R Cardenas J C Wade C E Holcomb J B Advances in the understanding of trauma-induced coagulopathy Blood 2016 128 8 1043 1049
18. Dobson G P Letson H L Sharma R Sheppard F R Cap A P Mechanisms of early trauma-induced coagulopathy: the clot thickens or not? J Trauma Acute Care Surg 2015 79 2 301 309
19. Ostrowski S R Sørensen A M Larsen C F Johansson P I Thrombelastography and biomarker profiles in acute coagulopathy of trauma: a prospective study Scand J Trauma Resusc Emerg Med 2011 19 64
20. Johansson P I Ostrowski S R Acute coagulopathy of trauma: balancing progressive catecholamine induced endothelial activation and damage by fluid phase anticoagulation Med Hypotheses 2010 75 6 564 567
21. Gando S Otomo Y Local hemostasis, immunothrombosis, and systemic disseminated intravascular coagulation in trauma and traumatic shock Crit Care 2015 19 72
22. Johansson P I Stensballe J Rosenberg I Hilsløv T L Jørgensen L Secher N H Proactive administration of platelets and plasma for patients with a ruptured abdominal aortic aneurysm: evaluating a change in transfusion practice Transfusion 2007 47 4 593 598
23. Frith D Goslings J C Gaarder C, et al. Definition and drivers of acute traumatic coagulopathy: clinical and experimental investigations J Thromb Haemost 2010 8 9 1919 1925
24. Maegele M The coagulopathy of trauma Eur J Trauma Emerg Surg 2014 40 2 113 126
25. Cap A Hunt B Acute traumatic coagulopathy Curr Opin Crit Care 2014 20 6 638 645
26. Howard B M Kornblith L Z Cheung C K, et al. Inducing acute traumatic coagulopathy in vitro: the effects of activated protein C on healthy human whole blood PLoS One 2016 11 3 e0150930
27. Cohen M J Call M Nelson M, et al. Critical role of activated protein C in early coagulopathy and later organ failure, infection and death in trauma patients Ann Surg 2012 255 2 379 385
28. Johansson P I Sørensen A M Perner A, et al. Disseminated intravascular coagulation or acute coagulopathy of trauma shock early after trauma? An observational study Crit Care 2011 15 (6, R272): R272
29. Cohen M J Kutcher M Redick B, et al; PROMMTT Study Group. Clinical and mechanistic drivers of acute traumatic coagulopathy J Trauma Acute Care Surg 2013 75 (1, Suppl 1): S40 S47
30. Feistritzer C Riewald M Endothelial barrier protection by activated protein C through PAR1-dependent sphingosine 1-phosphate receptor-1 cross activation Blood 2005 105 8 3178 3184
31. Sawamura A Hayakawa M Gando S, et al. Disseminated intravascular coagulation with a fibrinolytic phenotype at an early phase of trauma predicts mortality Thromb Res 2009 124 5 608 613
32. Oshiro A Yanagida Y Gando S Henzan N Takahashi I Makise H Hemostasis during the early stages of trauma: comparison with disseminated intravascular coagulation Crit Care 2014 18 2 R61
33. Chapman M P Moore E E Moore H B, et al. Overwhelming tPA release, not PAI-1 degradation, is responsible for hyperfibrinolysis in severely injured trauma patients J Trauma Acute Care Surg 2016 80 1 16 23, discussion 23-25
34. Gando S Sawamura A Hayakawa M Trauma, shock, and disseminated intravascular coagulation: lessons from the classical literature Ann Surg 2011 254 1 10 19
35. Moore H B Moore E E Gonzalez E, et al. Hyperfibrinolysis, physiologic fibrinolysis, and fibrinolysis shutdown: the spectrum of postinjury fibrinolysis and relevance to antifibrinolytic therapy J Trauma Acute Care Surg 2014 77 6 811 817, discussion 817
36. Bluth M H Kashuk J L Mechanistic links in trauma-induced coagulopathy: a tale of two cities Ann Surg 2011 254 1 20 21
37. Schlimp C J Voelckel W Inaba K Maegele M Schöchl H Impact of fibrinogen concentrate alone or with prothrombin complex concentrate (+/-fresh frozen plasma) on plasma fibrinogen level and fibrin-based clot strength (FIBTEM) in major trauma: a retrospective study Scand J Trauma Resusc Emerg Med 2013 21 74
38. Collins P W Solomon C Sutor K, et al. Theoretical modelling of fibrinogen supplementation with therapeutic plasma, cryoprecipitate, or fibrinogen concentrate Br J Anaesth 2014 113 4 585 595
39. Kashuk J L Moore E E Sawyer M, et al. Primary fibrinolysis is integral in the pathogenesis of the acute coagulopathy of trauma Ann Surg 2010 252 3 434 442, discussion 443-444
40. Ketchum L Hess J R Hiippala S Indications for early fresh frozen plasma, cryoprecipitate, and platelet transfusion in trauma J Trauma 2006 60 (6, Suppl): S51 S58
41. White N J Mechanisms of trauma-induced coagulopathy Hematology (Am Soc Hematol Educ Program) 2013 2013 13 660 663
42. Willoughby M L A puerperal haemorrhagic state due to a henarin-like anticoagulant J Clin Pathol 1963 16 108 111
43. Johansson P I Stensballe J Rasmussen L S Ostrowski S R A high admission syndecan-1 level, a marker of endothelial glycocalyx degradation, is associated with inflammation, protein C depletion, fibrinolysis, and increased mortality in trauma patients Ann Surg 2011 254 2 194 200
44. Ostrowski S R Johansson P I Endothelial glycocalyx degradation induces endogenous heparinization in patients with severe injury and early traumatic coagulopathy J Trauma Acute Care Surg 2012 73 1 60 66
45. Johansson P I Henriksen H H Stensballe J, et al. Traumatic endotheliopathy: a prospective observational study of 424 severely injured patients Ann Surg 2017 265 3 597 603
46. Rizoli S Nascimento B Jr Key N, et al. Disseminated intravascular coagulopathy in the first 24 hours after trauma: the association between ISTH score and anatomopathologic evidence J Trauma 2011 71 (5, Suppl 1): S441 S447
47. Vincent J L De Backer D Does disseminated intravascular coagulation lead to multiple organ failure? Crit Care Clin 2005 21 3 469 477
48. Franchini M Lippi G Manzato F Recent acquisitions in the pathophysiology, diagnosis and treatment of disseminated intravascular coagulation Thromb J 2006 4 4
49. Biemond B J Levi M Ten Cate H, et al. Plasminogen activator and plasminogen activator inhibitor I release during experimental endotoxaemia in chimpanzees: effect of interventions in the cytokine and coagulation cascades Clin Sci (Lond) 1995 88 5 587 594
50. van Hinsbergh V W Kooistra T van den Berg E A Princen H M Fiers W Emeis J J Tumor necrosis factor increases the production of plasminogen activator inhibitor in human endothelial cells in vitro and in rats in vivo Blood 1988 72 5 1467 1473
51. Mesters R M Flörke N Ostermann H Kienast J Increase of plasminogen activator inhibitor levels predicts outcome of leukocytopenic patients with sepsis Thromb Haemost 1996 75 6 902 907
52. Asakura H Ontachi Y Mizutani T, et al. An enhanced fibrinolysis prevents the development of multiple organ failure in disseminated intravascular coagulation in spite of much activation of blood coagulation Crit Care Med 2001 29 6 1164 1168
53. Levi M Disseminated intravascular coagulation in cancer patients Best Pract Res Clin Haematol 2009 22 1 129 136
54. Holley A D Reade M C The ‘procoagulopathy’ of trauma: too much, too late? Curr Opin Crit Care 2013 19 6 578 586
55. Pusateri A E Weiskopf R B Bebarta V, et al; US DoD Hemorrhage and Resuscitation Research and Development Steering Committee. Tranexamic acid and trauma: current status and knowledge gaps with recommended research priorities Shock 2013 39 2 121 126
56. Morrison J J Dubose J J Rasmussen T E Midwinter M J Military application of tranexamic acid in trauma emergency resuscitation (MATTERs) study Arch Surg 2012 147 2 113 119
57. Morrison J J Ross J D Dubose J J Jansen J O Midwinter M J Rasmussen T E Association of cryoprecipitate and tranexamic acid with improved survival following wartime injury: findings from the MATTERs II Study JAMA Surg 2013 148 3 218 225
58. MacDonald S G Luddington R J Critical factors contributing to the thromboelastography trace Semin Thromb Hemost 2010 36 7 712 722
59. Gruen R L Jacobs I G Reade M C; PATCH-Trauma study. Trauma and tranexamic acid Med J Aust 2013 199 5 310 311
60. Rossaint R Bouillon B Cerny V, et al. The European guideline on management of major bleeding and coagulopathy following trauma: fourth edition Crit Care 2016 20 100
61. Mutch N Booth N Plasmin-antiplasmin system In: Gonzalez E Moore H Moore E, eds. Trauma Induced Coagulopathy Switzerland Springer International Publishing 2016 31 51
62. Medcalf R L The traumatic side of fibrinolysis Blood 2015 125 16 2457 2458
63. Hijazi N Abu Fanne R Abramovitch R, et al. Endogenous plasminogen activators mediate progressive intracerebral hemorrhage after traumatic brain injury in mice Blood 2015 125 16 2558 2567
64. Inaba K Rizoli S Veigas P V, et al; Viscoelastic Testing in Trauma Consensus Panel. 2014 Consensus conference on viscoelastic test-based transfusion guidelines for early trauma resuscitation: report of the panel J Trauma Acute Care Surg 2015 78 6 1220 1229
65. Schöchl H Voelckel W Grassetto A Schlimp C J Practical application of point-of-care coagulation testing to guide treatment decisions in trauma J Trauma Acute Care Surg 2013 74 6 1587 1598
66. Holcomb J B Minei K M Scerbo M L, et al. Admission rapid thrombelastography can replace conventional coagulation tests in the emergency department: experience with 1974 consecutive trauma patients Ann Surg 2012 256 3 476 486
67. Stensballe J Ostrowski S R Johansson P I Viscoelastic guidance of resuscitation Curr Opin Anaesthesiol 2014 27 2 212 218
68. Johansson P I Stissing T Bochsen L Ostrowski S R Thrombelastography and thromboelastometry in assessing coagulopathy in trauma Scand J Trauma Resusc Emerg Med 2009 17 45
69. Kashuk J L Moore E E Sawyer M, et al. Postinjury coagulopathy management: goal directed resuscitation via POC thrombelastography Ann Surg 2010 251 4 604 614
70. Schöchl H Maegele M Voelckel W Fixed ratio versus goal-directed therapy in trauma Curr Opin Anaesthesiol 2016 29 2 234 244
71. Harr J N Moore E E Ghasabyan A, et al. Functional fibrinogen assay indicates that fibrinogen is critical in correcting abnormal clot strength following trauma Shock 2013 39 1 45 49
72. Holcomb J B Tilley B C Baraniuk S, et al; PROPPR Study Group. Transfusion of plasma, platelets, and red blood cells in a 1:1:1 vs a 1:1:2 ratio and mortality in patients with severe trauma: the PROPPR randomized clinical trial JAMA 2015 313 5 471 482
73. Theusinger O M Stein P Levy J H Point of care and factor concentrate-based coagulation algorithms Transfus Med Hemother 2015 42 2 115 121
74. Gonzalez E Moore E E Moore H B, et al. Goal-directed hemostatic resuscitation of trauma-induced coagulopathy: a pragmatic randomized clinical trial comparing a viscoelastic assay to conventional coagulation assays Ann Surg 2016 263 6 1051 1059
75. Solomon C Schöchl H Ranucci M Schlimp C J Can the viscoelastic parameter α-angle distinguish fibrinogen from platelet deficiency and guide fibrinogen supplementation? Anesth Analg 2015 121 2 289 301
76. McCurdy M T Liew-Spilger A Walsh M Mortality and ratio of blood products used in patients with sever e trauma. (Letter) JAMA 2015 313 20 2077 2078
77. Moore H B Moore E E Gonzalez E Mortality and ratio of blood products used in patients with severe traum a. (Letter) JAMA 2015 313 20 2077
78. Moore E E Chin T L Chapman M C, et al. Plasma first in the field for postinjury hemorrhagic shock Shock 2014 41 01 35 38
79. Moore H B Moore E E Morton A P, et al. Shock-induced systemic hyperfibrinolysis is attenuated by plasma-first resuscitation J Trauma Acute Care Surg 2015 79 6 897 903, discussion 903-904
80. Moore H B Moore E E Chapman M P, et al. Viscoelastic measurements of platelet function, not fibrinogen function, predicts sensitivity to tissue-type plasminogen activator in trauma patients J Thromb Haemost 2015 13 10 1878 1887
81. Wohlauer M V Moore E E Thomas S, et al. Early platelet dysfunction: an unrecognized role in the acute coagulopathy of trauma J Am Coll Surg 2012 214 5 739 746
82. Cole E Davenport R Willett K Brohi K Tranexamic acid use in severely injured civilian patients and the effects on outcomes: a prospective cohort study Ann Surg 2015 261 2 390 394
83. Wafaisade A Lefering R Bouillon B Böhmer A B Gäßler M Ruppert M; TraumaRegister DGU. Prehospital administration of tranexamic acid in trauma patients Crit Care 2016 20 1 143
84. Moore H B Moore E E Liras I N, et al. Acute fibrinolysis shutdown after injury occurs frequently and increases mortality: a multicenter evaluation of 2,540 severely injured patients J Am Coll Surg 2016 222 4 347 355
85. Ausset S Glassberg E Nadler R, et al. Tranexamic acid as part of remote damage-control resuscitation in the prehospital setting: A critical appraisal of the medical literature and available alternatives J Trauma Acute Care Surg 2015 78 (6, Suppl 1): S70 S75
86. Moore H Moore E Gonzalez E Fibrinolysis In: Gonzalez E Moore H Moore E, eds. Trauma Induced Coagulopathy Switzerland Springer International Publishing 2016 135 147
87. Moore E E Moore H B Gonzalez E Sauaia A Banerjee A Silliman C C Rationale for the selective administration of tranexamic acid to inhibit fibrinolysis in the severely injured patient Transfusion 2016 56 02 S110 S114
88. Chakrabarti R Hocking E D Fearnley G R Reaction pattern to three stresses--electroplexy, surgery, and myocardial infarction--of fibrinolysis and plasma fibrinogen J Clin Pathol 1969 22 6 659 662
89. Griffiths N J Factors affecting the fibrinolytic response to surgery Ann R Coll Surg Engl 1979 61 1 12 16
90. Yukizawa Y Inaba Y Watanabe S, et al. Association between venous thromboembolism and plasma levels of both soluble fibrin and plasminogen-activator inhibitor 1 in 170 patients undergoing total hip arthroplasty Acta Orthop 2012 83 1 14 21
91. Schneeweiss S Seeger J D Landon J Walker A M Aprotinin during coronary-artery bypass grafting and risk of death N Engl J Med 2008 358 8 771 783
92. Groth C G Pechet L Starzl T E Coagulation during and after orthotopic transplantation of the human liver Arch Surg 1969 98 1 31 34
93. Kang Y G Martin D J Marquez J, et al. Intraoperative changes in blood coagulation and thromboelastographic monitoring in liver transplantation Anesth Analg 1985 64 9 888 896
94. Gando S Nakanishi Y Tedo I Cytokines and plasminogen activator inhibitor-1 in posttrauma disseminated intravascular coagulation: relationship to multiple organ dysfunction syndrome Crit Care Med 1995 23 11 1835 1842
95. Ostrowski S R Berg R M Windeløv N A, et al. Discrepant fibrinolytic response in plasma and whole blood during experimental endotoxemia in healthy volunteers PLoS One 2013 8 3 e59368
96. Bachofen M Weibel E R Structural alterations of lung parenchyma in the adult respiratory distress syndrome Clin Chest Med 1982 3 1 35 56
97. Ogston D Ogston C M Ratnoff O D Forbes C D Studies on a complex mechanism for the activation of plasminogen by kaolin and by chloroform: the participation of Hageman factor and additional cofactors J Clin Invest 1969 48 10 1786 1801
98. Zufferey P J Miquet M Quenet S, et al; Tranexamic Acid in Hip-Fracture Surgery (THIF) Study. Tranexamic acid in hip fracture surgery: a randomized controlled trial Br J Anaesth 2010 104 1 23 30
99. Kluft C Verheijen J H Jie A F, et al. The postoperative fibrinolytic shutdown: a rapidly reverting acute phase pattern for the fast-acting inhibitor of tissue-type plasminogen activator after trauma Scand J Clin Lab Invest 1985 45 7 605 610
100. Kassis J Hirsh J Podor T J Evidence that postoperative fibrinolytic shutdown is mediated by plasma factors that stimulate endothelial cell type I plasminogen activator inhibitor biosynthesis Blood 1992 80 7 1758 1764
101. Castellino F J Chapman M P Donahue D L, et al. Traumatic brain injury causes platelet adenosine diphosphate and arachidonic acid receptor inhibition independent of hemorrhagic shock in humans and rats J Trauma Acute Care Surg 2014 76 5 1169 1176
102. Sashindranath M Sales E Daglas M, et al. The tissue-type plasminogen activator-plasminogen activator inhibitor 1 complex promotes neurovascular injury in brain trauma: evidence from mice and humans Brain 2012 135 (Pt 11): 3251 3264
103. Chapman M P Moore E E Ramos C R, et al. Fibrinolysis greater than 3% is the critical value for initiation of antifibrinolytic therapy J Trauma Acute Care Surg 2013 75 6 961 967, discussion 967
104. Schöchl H Voelckel W Maegele M Solomon C Trauma-associated hyperfibrinolysis Hamostaseologie 2012 32 1 22 27
105. Schöchl H Frietsch T Pavelka M Jámbor C Hyperfibrinolysis after major trauma: differential diagnosis of lysis patterns and prognostic value of thromboelastometry J Trauma 2009 67 1 125 131
106. Theusinger O M Wanner G A Emmert M Y, et al. Hyperfibrinolysis diagnosed by rotational thromboelastometry (ROTEM) is associated with higher mortality in patients with severe trauma Anesth Analg 2011 113 5 1003 1012
107. Tapia N M Chang A Norman M, et al. TEG-guided resuscitation is superior to standardized MTP resuscitation in massively transfused penetrating trauma patients J Trauma Acute Care Surg 2013 74 2 378 385, discussion 385-386
108. Li R Elmongy H Sims C Diamond S L Ex vivo recapitulation of trauma-induced coagulopathy and preliminary assessment of trauma patient platelet function under flow using microfluidic technology J Trauma Acute Care Surg 2016 80 3 440 449
109. Raza I Davenport R Rourke C, et al. The incidence and magnitude of fibrinolytic activation in trauma patients J Thromb Haemost 2013 11 2 307 314
110. Ramos C R Moore E E Manco-Johnson M L Silliman C C Chapman M C Banerjee A The incidence and magnitude of fibrinolytic activation in trauma patients: a rebuttal J Thromb Haemost 2013 11 7 1435 1437
111. Larsen O H Fenger-Eriksen C Ingerslev J Sørensen B Improved point-of-care identification of hyperfibrinolysis is needed Thromb Res 2012 130 4 690 691
112. Hunt B J Raza I Brohi K The incidence and magnitude of fibrinolytic activation in trauma patients: a reply to a rebuttal J Thromb Haemost 2013 11 7 1437 1438
113. Johansson P I Stensballe J Oliveri R Wade C E Ostrowski S R Holcomb J B How I treat patients with massive hemorrhage Blood 2014 124 20 3052 3058
114. Schöchl H Maegele M Solomon C Görlinger K Voelckel W Early and individualized goal-directed therapy for trauma-induced coagulopathy Scand J Trauma Resusc Emerg Med 2012 20 15
115. Branco B C Inaba K Ives C, et al. Thromboelastogram evaluation of the impact of hypercoagulability in trauma patients Shock 2014 41 3 200 207
116. Schlimp C J Solomon C Ranucci M Hochleitner G Redl H Schöchl H The effectiveness of different functional fibrinogen polymerization assays in eliminating platelet contribution to clot strength in thromboelastometry Anesth Analg 2014 118 2 269 276
117. Johansson P I Sørensen A M Larsen C F, et al. Low hemorrhage-related mortality in trauma patients in a Level I trauma center employing transfusion packages and early thromboelastography-directed hemostatic resuscitation with plasma and platelets Transfusion 2013 53 12 3088 3099
118. Johansson P I Stensballe J Rasmussen L S Ostrowski S R High circulating adrenaline levels at admission predict increased mortality after trauma J Trauma Acute Care Surg 2012 72 2 428 436
119. Kutcher M E Redick B J McCreery R C, et al. Characterization of platelet dysfunction after trauma J Trauma Acute Care Surg 2012 73 1 13 19
120. Solomon C Traintinger S Ziegler B, et al. Platelet function following trauma. A multiple electrode aggregometry study Thromb Haemost 2011 106 2 322 330
121. Chandler W L Procoagulant activity in trauma patients Am J Clin Pathol 2010 134 1 90 96
122. Adamzik M Eggmann M Frey U H, et al. Comparison of thromboelastometry with procalcitonin, interleukin 6, and C-reactive protein as diagnostic tests for severe sepsis in critically ill adults Crit Care 2010 14 5 R178
123. Ostrowski S R Haase N Müller R B, et al. Association between biomarkers of endothelial injury and hypocoagulability in patients with severe sepsis: a prospective study Crit Care 2015 19 191