Activated Protein C Drives the Hyperfibrinolysis of Acute Traumatic Coagulopathy

Anesthesiology

Volumn 126, Issue 1, 2017, Pages 115-127

  Davenport, Ross A ^a   Guerreiro, Maria ^a   Frith, Daniel ^a   Rourke, Claire ^a   Platton, Sean ^b   Cohen, Mitchell ^c   Pearse, Rupert ^a   Thiemermann, Chris ^a   Brohi, Karim ^a  

^a QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

^b BARTS HEALTH NHS TRUST   (United Kingdom)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVATED PROTEIN C; FIBRINOGEN; PROTHROMBIN; TISSUE PLASMINOGEN ACTIVATOR; VON WILLEBRAND FACTOR; PROTEIN C;

ACUTE TRAUMATIC COAGULOPATHY; ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BLOOD CLOTTING DISORDER; COHORT ANALYSIS; CONTROLLED STUDY; EMERGENCY HEALTH SERVICE; FEMALE; FIBRINOGENOLYSIS; FIBRINOLYSIS; HEMODILUTION; HUMAN; INJURY; INJURY SCALE; MAJOR CLINICAL STUDY; MALE; MEAN ARTERIAL PRESSURE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROSPECTIVE STUDY; PROTEIN BLOOD LEVEL; PROTEIN EXPRESSION; PROTHROMBIN TIME; ANIMAL; BLEEDING; BLOOD; BLOOD CLOTTING; BLOOD CLOTTING TEST; DISEASE MODEL; METABOLISM; MIDDLE AGED; PATHOPHYSIOLOGY; PHYSIOLOGY; STATISTICS AND NUMERICAL DATA; THROMBOELASTOGRAPHY; YOUNG ADULT;

ADULT; ANIMALS; BLOOD COAGULATION; BLOOD COAGULATION TESTS; COHORT STUDIES; DISEASE MODELS, ANIMAL; FEMALE; FIBRINOGEN; FIBRINOLYSIS; HEMORRHAGE; HUMANS; MALE; MICE; MIDDLE AGED; PROSPECTIVE STUDIES; PROTEIN C; THROMBELASTOGRAPHY; WOUNDS AND INJURIES; YOUNG ADULT;

EID: 84995428291     PISSN: 00033022     EISSN: 15281175     Source Type: Journal    
DOI: 10.1097/ALN.0000000000001428     Document Type: Article

References (57)

1. Bickell WH, Wall MJ Jr, Pepe PE, Martin RR, Ginger VF, Allen MK, Mattox KL: Immediate versus delayed fluid resuscitation for hypotensive patients with penetrating torso injuries. N Engl J Med 1994; 331:1105-9
2. Gruen RL, Jurkovich GJ, McIntyre LK, Foy HM, Maier RV: Patterns of errors contributing to trauma mortality: Lessons learned from 2,594 deaths. Ann Surg 2006; 244:371-80
3. Kauvar DS, Lefering R, Wade CE: Impact of hemorrhage on trauma outcome: An overview of epidemiology, clinical presentations, and therapeutic considerations. J Trauma 2006; 60(6 Suppl):S3-11
4. Brohi K, Singh J, Heron M, Coats T: Acute traumatic coagulopathy. J Trauma 2003; 54:1127-30
5. MacLeod JB, Lynn M, McKenney MG, Cohn SM, Murtha M: Early coagulopathy predicts mortality in trauma. J Trauma 2003; 55:39-44
6. Maegele M, Lefering R, Yucel N, Tjardes T, Rixen D, Paffrath T, Simanski C, Neugebauer E, Bouillon B; AG Polytrauma of the German Trauma Society (DGU): Early coagulopathy in multiple injury: An analysis from the German Trauma Registry on 8724 patients. Injury 2007; 38:298-304
7. Brohi K, Cohen MJ, Ganter MT, Matthay MA, Mackersie RC, Pittet JF: Acute traumatic coagulopathy: Initiated by hypoperfusion: Modulated through the protein C pathway? Ann Surg 2007; 245:812-8
8. Gruen RL, Brohi K, Schreiber M, Balogh ZJ, Pitt V, Narayan M, Maier RV: Haemorrhage control in severely injured patients. Lancet 2012; 380:1099-108
9. Cohen MJ, Brohi K, Ganter MT, Manley GT, Mackersie RC, Pittet JF: Early coagulopathy after traumatic brain injury: The role of hypoperfusion and the protein C pathway. J Trauma 2007; 63:1254-61; discussion 1261-2
10. Hayakawa M, Gando S, Ieko M, Honma Y, Homma T, Yanagida Y, Kubota N, Uegaki S, Sawamura A, Asakura H: Massive amounts of tissue factor induce fibrinogenolysis without tissue hypoperfusion in rats. Shock 2013; 39:514-9
11. Johansson PI, Sørensen AM, Perner A, Welling KL, Wanscher M, Larsen CF, Ostrowski SR: Disseminated intravascular coagulation or acute coagulopathy of trauma shock early after trauma? An observational study. Crit Care 2011; 15:R272
12. Rizoli S, Nascimento B Jr, Key N, Tien HC, Muraca S, Pinto R, Khalifa M, Plotkin A, Callum J: 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):S441-7
13. Gando S, Sawamura A, Hayakawa M: Trauma, shock, and disseminated intravascular coagulation: Lessons from the classical literature. Ann Surg 2011; 254:10-9
14. Dobson GP, Letson HL, Sharma R, Sheppard FR, Cap AP: Mechanisms of early trauma-induced coagulopathy: The clot thickens or not? J Trauma Acute Care Surg 2015; 79:301-9
15. Floccard B, Rugeri L, Faure A, Saint Denis M, Boyle EM, Peguet O, Levrat A, Guillaume C, Marcotte G, Vulliez A, Hautin E, David JS, Négrier C, Allaouchiche B: Early coagulopathy in trauma patients: An on-scene and hospital admission study. Injury 2012; 43:26-32
16. Davenport R, Manson J, De'Ath H, Platton S, Coates A, Allard S, Hart D, Pearse R, Pasi KJ, MacCallum P, Stanworth S, Brohi K: Functional definition and characterization of acute traumatic coagulopathy. Crit Care Med 2011; 39:2652-8
17. Cohen MJ, Kutcher M, Redick B, Nelson M, Call M, Knudson MM, Schreiber MA, Bulger EM, Muskat P, Alarcon LH, Myers JG, Rahbar MH, Brasel KJ, Phelan HA, del Junco DJ, Fox EE, Wade CE, Holcomb JB, Cotton BA, Matijevic N; PROMMTT Study Group: Clinical and mechanistic drivers of acute traumatic coagulopathy. J Trauma Acute Care Surg 2013; 75(1 Suppl 1):S40-7
18. Johansson PI, Stensballe J, Rasmussen LS, Ostrowski SR: 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; 254:194-200
19. Frith D, Cohen MJ, Brohi K: Animal models of traumainduced coagulopathy. Thromb Res 2012; 129:551-6
20. Frith D, Goslings JC, Gaarder C, Maegele M, Cohen MJ, Allard S, Johansson PI, Stanworth S, Thiemermann C, Brohi K: Definition and drivers of acute traumatic coagulopathy: Clinical and experimental investigations. J Thromb Haemost 2010; 8:1919-25
21. Raza I, Davenport R, Rourke C, Platton S, Manson J, Spoors C, Khan S, De'Ath HD, Allard S, Hart DP, Pasi KJ, Hunt BJ, Stanworth S, MacCallum PK, Brohi K: The incidence and magnitude of fibrinolytic activation in trauma patients. J Thromb Haemost 2013; 11:307-14
22. Kashuk JL, Moore EE, Sawyer M, Wohlauer M, Pezold M, Barnett C, Biffl WL, Burlew CC, Johnson JL, Sauaia A: Primary fibrinolysis is integral in the pathogenesis of the acute coagulopathy of trauma. Ann Surg 2010; 252:434-42; discussion 443-4
23. Hagemo JS, Stanworth S, Juffermans NP, Brohi K, Cohen M, Johansson PI, Røislien J, Eken T, Nass PA, Gaarder C: Prevalence, predictors and outcome of hypofibrinogenaemia in trauma: A multicentre observational study. Crit Care 2014; 18:R52
24. Rourke C, Curry N, Khan S, Taylor R, Raza I, Davenport R, Stanworth S, Brohi K: Fibrinogen levels during trauma hemorrhage, response to replacement therapy, and association with patient outcomes. J Thromb Haemost 2012; 10:1342-51
25. Brohi K, Cohen MJ, Ganter MT, Schultz MJ, Levi M, Mackersie RC, Pittet JF: Acute coagulopathy of trauma: Hypoperfusion induces systemic anticoagulation and hyperfibrinolysis. J Trauma 2008; 64:1211-7; discussion 1217
26. Rezaie AR: Vitronectin functions as a cofactor for rapid inhibition of activated protein C by plasminogen activator inhibitor-1. Implications for the mechanism of profibrinolytic action of activated protein C. J Biol Chem 2001; 276:15567-70
27. Dunbar NM, Chandler WL: Thrombin generation in trauma patients. Transfusion 2009; 49:2652-60
28. Hunt BJ, Jurd KM: Endothelial cell activation. A central pathophysiological process. BMJ 1998; 316:1328-9
29. Eastridge BJ, Malone D, Holcomb JB: Early predictors of transfusion and mortality after injury: A review of the databased literature. J Trauma 2006; 60(6 Suppl):S20-5
30. Davis JW, Parks SN, Kaups KL, Gladen HE, O'Donnell-Nicol S: Admission base deficit predicts transfusion requirements and risk of complications. J Trauma 1996; 41:769-74
31. Cohen MJ, Call M, Nelson M, Calfee CS, Esmon CT, Brohi K, Pittet JF: Critical role of activated protein C in early coagulopathy and later organ failure, infection and death in trauma patients. Ann Surg 2012; 255:379-85
32. Gruber A, Griffin JH: Direct detection of activated protein C in blood from human subjects. Blood 1992; 79:2340-8
33. Kaiser B, Jeske W, Hoppensteadt DH, Walenga JM, Drohan W, Fareed J: In vitro studies on the effect of activated protein C on platelet activation and thrombin generation. Thromb Res 1997; 87:197-204
34. Hemker HC, Giesen P, AlDieri R, Regnault V, de Smed E, Wagenvoord R, Lecompte T, Béguin S: The calibrated automated thrombogram (CAT): A universal routine test for hyperand hypocoagulability. Pathophysiol Haemost Thromb 2002; 32:249-53
35. Chesebro BB, Rahn P, Carles M, Esmon CT, Xu J, Brohi K, Frith D, Pittet JF, Cohen MJ: Increase in activated protein C mediates acute traumatic coagulopathy in mice. Shock 2009; 32:659-65
36. Cohen MJ, Bir N, Rahn P, Dotson R, Brohi K, Chesebro BB, Mackersie R, Carles M, Wiener-Kronish J, Pittet JF: Protein C depletion early after trauma increases the risk of ventilatorassociated pneumonia. J Trauma 2009; 67:1176-81
37. Ostrowski SR, Sørensen AM, Larsen CF, Johansson PI: Thrombelastography and biomarker profiles in acute coagulopathy of trauma: A prospective study. Scand J Trauma Resusc Emerg Med 2011; 19:64
38. Tripodi A, Chantarangkul V, Mannucci PM: Acquired coagulation disorders: Revisited using global coagulation/anticoagulation testing. Br J Haematol 2009; 147:77-82
39. Cardenas JC, Rahbar E, Pommerening MJ, Baer LA, Matijevic N, Cotton BA, Holcomb JB, Wade CE: Measuring thrombin generation as a tool for predicting hemostatic potential and transfusion requirements following trauma. J Trauma Acute Care Surg 2014; 77:839-45
40. 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; 11:826-35
41. 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:R61
42. Stinger HK, Spinella PC, Perkins JG, Grathwohl KW, Salinas J, Martini WZ, Hess JR, Dubick MA, Simon CD, Beekley AC, Wolf SE, Wade CE, Holcomb JB: The ratio of fibrinogen to red cells transfused affects survival in casualties receiving massive transfusions at an army combat support hospital. J Trauma 2008; 64(2 Suppl):S79-85; discussion S85
43. Schlimp CJ, 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
44. Curry N, Rourke C, Davenport R, Beer S, Pankhurst L, Deary A, Thomas H, Llewelyn C, Green L, Doughty H, Nordmann G, Brohi K, Stanworth S: Early cryoprecipitate for major haemorrhage in trauma: A randomised controlled feasibility trial. Br J Anaesth 2015; 115:76-83
45. Spahn DR, Bouillon B, Cerny V, Coats TJ, Duranteau J, Fernández-Mondéjar E, Filipescu D, Hunt BJ, Komadina R, Nardi G, Neugebauer E, Ozier Y, Riddez L, Schultz A, Vincent JL, Rossaint R: Management of bleeding and coagulopathy following major trauma: An updated European guideline. Crit Care 2013; 17:R76
46. Gaffney PJ: Fibrin(-ogen) interactions with plasmin. Haemostasis 1977; 6:2-25
47. Boldt J, Papsdorf M, Rothe A, Kumle B, Piper S: Changes of the hemostatic network in critically ill patients-is there a difference between sepsis, trauma, and neurosurgery patients? Crit Care Med 2000; 28:445-50
48. Liaw PC, Esmon CT, Kahnamoui K, Schmidt S, Kahnamoui S, Ferrell G, Beaudin S, Julian JA, Weitz JI, Crowther M, Loeb M, Cook D: Patients with severe sepsis vary markedly in their ability to generate activated protein C. Blood 2004; 104:3958-64
49. Mesters RM, Helterbrand J, Utterback BG, Yan B, Chao YB, Fernandez JA, Griffin JH, Hartman DL: Prognostic value of protein C concentrations in neutropenic patients at high risk of severe septic complications. Crit Care Med 2000; 28:2209-16
50. Asaka S, Shibayama Y, Nakata K: Pathogenesis of focal and random hepatocellular necrosis in endotoxemia: Microscopic observation in vivo. Liver 1996; 16:183-7
51. Esmon CT: Inflammation and the activated protein C anticoagulant pathway. Semin Thromb Hemost 2006; 32 Suppl 1:49-60
52. Stanworth SJ, Hyde CJ, Murphy MF: Evidence for indications of fresh frozen plasma. Transfus Clin Biol 2007; 14:551-6
53. Khan S, Brohi K, Chana M, Raza I, Stanworth S, Gaarder C, Davenport R; International Trauma Research Network (INTRN): Hemostatic resuscitation is neither hemostatic nor resuscitative in trauma hemorrhage. J Trauma Acute Care Surg 2014; 76:561-7; discussion 7-8
54. Shakur H, Roberts I, Bautista R, Caballero J, Coats T, Dewan Y, El-Sayed H, Gogichaishvili T, Gupta S, Herrera J, Hunt B, Iribhogbe P, Izurieta M, Khamis H, Komolafe E, Marrero MA, Mejia-Mantilla J, Miranda J, Morales C, Olaomi O, Olldashi F, Perel P, Peto R, Ramana PV, Ravi RR, Yutthakasemsunt S: 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
55. Ausset S, Glassberg E, Nadler R, Sunde G, Cap AP, Hoffmann C, Plang S, Sailliol A: 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):S70-5
56. Morrison JJ, Dubose JJ, Rasmussen TE, Midwinter MJ: Military Application of Tranexamic Acid in Trauma Emergency Resuscitation (MATTERs) Study. Arch Surg 2012; 147:113-9
57. 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; 261:390-4