Thrombin in Myocardial Ischemia-Reperfusion During Cardiac Surgery

Annals of Thoracic Surgery

Volumn 88, Issue 1, 2009, Pages 318-325

  Raivio, Peter ^a   Lassila, Riitta ^a   Petäjä, Jari ^a  

^a HELSINKI UNIVERSITY CENTRAL HOSPITAL   (Finland)

Author keywords

[No Author keywords available]

Indexed keywords

THROMBIN;

APOPTOSIS; BLOOD CLOTTING; CARDIOPULMONARY BYPASS; CLINICAL FEATURE; CORONARY ARTERY THROMBOSIS; FIBRINOLYSIS; HEART MUSCLE CELL; HEART MUSCLE ISCHEMIA; HUMAN; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; REPERFUSION INJURY; REVIEW;

ANIMALS; ANTICOAGULANTS; BIOLOGICAL MARKERS; CARDIAC SURGICAL PROCEDURES; CARDIOPULMONARY BYPASS; CORONARY ARTERY BYPASS; FEMALE; HUMANS; INTRAOPERATIVE COMPLICATIONS; MALE; MYOCARDIAL REPERFUSION; MYOCARDIAL REPERFUSION INJURY; PROGNOSIS; RISK ASSESSMENT; SENSITIVITY AND SPECIFICITY; SURVIVAL ANALYSIS; THROMBIN; TREATMENT OUTCOME;

EID: 67649792228     PISSN: 00034975     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.athoracsur.2008.12.097     Document Type: Review

References (93)

1. Lane D.A., Philippou H., and Huntington J.A. Directing thrombin. Blood 106 (2005) 2605-2612
2. Esmon C.T. The interactions between inflammation and coagulation. Br J Haematol 131 (2005) 417-430
3. Rossignol P., Bouton M.C., Jandrot-Perrus M., et al. A paradoxical pro-apoptotic effect of thrombin on smooth muscle cells. Exp Cell Res 299 (2004) 279-285
4. Edmunds Jr. L.H., and Colman R.W. Thrombin during cardiopulmonary bypass. Ann Thorac Surg 82 (2006) 2315-2322
5. Dutton R.C., and Edmunds Jr. L.H. Formation of platelet aggregate emboli in a prototype hollow fiber membrane oxygenator. J Biomed Mater Res 8 (1974) 163-183
6. Dutton R.C., Edmunds Jr. L.H., Hutchinson J.C., and Roe B.B. Platelet aggregate emboli produced in patients during cardiopulmonary bypass with membrane and bubble oxygenators and blood filters. J Thorac Cardiovasc Surg 67 (1974) 258-265
7. Blauth C.I., Arnold J.V., Schulenberg W.E., McCartney A.C., and Taylor K.M. Cerebral microembolism during cardiopulmonary bypass. Retinal microvascular studies in vivo with fluorescein angiography. J Thorac Cardiovasc Surg 95 (1988) 668-676
8. Raivio P., Kuitunen A., Suojaranta-Ylinen R., Lassila R., and Petäjä J. Thrombin generation during reperfusion after coronary artery bypass surgery associates with postoperative myocardial damage. J Thromb Haemost 4 (2006) 1523-1529
9. Croce K., and Libby P. Intertwining of thrombosis and inflammation in atherosclerosis. Curr Opin Hematol 14 (2007) 55-61
10. Herbert J.M., Dupuy E., Laplace M.C., Zini J.M., Bar Shavit R., and Tobelem G. Thrombin induces endothelial cell growth via both a proteolytic and a non-proteolytic pathway. Biochem J 303 (1994) 227-231
11. Patterson C., Stouffer G.A., Madamanchi N., and Runge M.S. New tricks for old dogs: Nonthrombotic effects of thrombin in vessel wall biology. Circ Res 88 (2001) 987-997
12. Chen L.B., and Buchanan J.M. Mitogenic activity of blood components. I. Thrombin and prothrombin. Proc Natl Acad Sci U S A 72 (1975) 131-135
13. Sobel B.E., Zaman T., Budd R.C., Schneider D.J., and Taatjes D.J. Attenuation of apoptosis and the eye of the beholder. Coronary Artery Dis 19 (2008) 55-58
14. Donovan F.M., and Cunningham D.D. Signalling pathways involved in thrombin-induced cell protection. J Biol Chem 273 (1998) 12746-12752
15. Zain J., Huang Y.Q., Feng X., Nierodzik M.L., Li J.J., and Karpatkin S. Concentration-dependent dual effect of thrombin on impaired growth/apoptosis or mitogenesis in tumor cells. Blood 95 (2000) 3133-3138
16. Leytin V., Allen D.J., Mykhaylov S., Lyubimov E., and Freedman J. Thrombin-triggered platelet apoptosis. J Thromb Haemost 4 (2006) 2656-2663
17. Leung R., Gwozdz A.M., Wang H., et al. Persistence of procoagulant surface expression on activated human platelets: Involvement of apoptosis and aminophospholipid translocase activity. J Thromb Haemost 5 (2007) 560-570
18. Liu D., Cheng T., Guo H., et al. Tissue plasminogen activator neurovascular toxicity is controlled by activated protein C. Nat Med 10 (2004) 1379-1383
19. Libby P. The molecular mechanisms of the thrombotic complications of atherosclerosis. J Intern Med 263 (2008) 517-527
20. Burke A.P., Kolodgie F.D., Farb A., et al. Healed plaque ruptures and sudden coronary death: Evidence that subclinical rupture has a role in plaque progression. Circulation 103 (2001) 934-940
21. Mann J., and Davies M.J. Mechanisms of progression in native coronary artery disease: role of healed plaque disruption. Heart 82 (1999) 265-268
22. Murphy E., and Steenbergen C. Mechanisms underlying acute protection from cardiac ischemiareperfusion injury. Physiol Rev 88 (2008) 581-609
23. Yellon D.M., and Hausenloy D.J. Myocardial reperfusion injury. N Engl J Med 357 (2007) 1121-1135
24. Mirabet M., Garcia-Dorado D., Ruiz-Meana M., Barrabes J.A., and Soler-Soler J. Thrombin increases cardiomyocyte acute cell death after ischemia and reperfusion. J Mol Cell Cardiol 39 (2005) 277-283
25. Erlich J.H., Boyle E.M., Labriola J., et al. Inhibition of the tissue factor-thrombin pathway limits infarct size after myocardial ischemia-reperfusion injury by reducing inflammation. Am J Pathol 157 (2000) 1849-1862
26. Strande J.L., Hsu A., Su J., Fu X., Gross G.J., and Baker J.E. SCH 79797, a selective PAR1 antagonist, limits myocardial ischemia/reperfusion injury in rat hearts. Basic Res Cardiol 102 (2007) 350-358
27. Golino P., Ragni M., Cirillo P., et al. Recombinant human, active site-blocked factor VIIa reduces infarct size and no-reflow phenomenon in rabbits. Am J Physiol Heart Circul Physiol 278 (2000) H1507-H1516
28. Jormalainen M., Vento A.E., Wartiovaara-Kautto U., Suojaranta-Ylinen R., Rämö O.J., and Petäjä J. Recombinant hirudin enhances cardiac output and decreases systemic vascular resistance during reperfusion after cardiopulmonary bypass in a porcine model. J Thorac Cardiovasc Surg 128 (2004) 189-196
29. Jormalainen M., Vento A.E., Lukkarinen H., et al. Inhibition of thrombin during reperfusion improves immediate postischemic myocardial function and modulates apoptosis in a porcine model of cardiopulmonary bypass. J Cardiothorac Vasc Anesth 21 (2007) 224-231
30. Snow T.R., Deal M.T., Dickey D.T., and Esmon C.T. Protein C activation following coronary artery occlusion in the in situ porcine heart. Circulation 84 (1991) 293-299
31. Ostrovsky L., Woodman R.C., Payne D., Teoh D., and Kubes P. Antithrombin III prevents and rapidly reverses leukocyte recruitment in ischemia/reperfusion. Circulation 96 (1997) 2302-2310
32. Schoots I.G., Levi M., van Vliet A.K., Maas A.M., Roossink E.H., and van Gulik T.M. Inhibition of coagulation and inflammation by activated protein C or antithrombin reduces intestinal ischemia/reperfusion injury in rats. Crit Care Med 32 (2004) 1375-1383
33. Yamaguchi Y., Okabe K., Liang J., et al. Thrombin and factor Xa enhance neutrophil chemoattractant production after ischemia/reperfusion in the rat liver. J Surg Res 92 (2000) 96-102
34. Yoshimura N., Kobayashi Y., Nakamura K., Yamagishi H., and Oka T. The effect of tissue factor pathway inhibitor on hepatic ischemic reperfusion injury of the rat. Transplantation 67 (1999) 45-53
35. Koudsi B., Chatman D.M., Ballinger B.A., et al. Tissue factor pathway inhibitor protects the ischemic spinal cord. J Surg Res 63 (1996) 174-178
36. Shibata M., Kumar S.R., Amar A., et al. Anti-inflammatory, antithrombotic, and neuroprotective effects of activated protein C in a murine model of focal ischemic stroke. Circulation 103 (2001) 1799-1805
37. Cheng T., Liu D., Griffin J.H., et al. Activated protein C blocks p53-mediated apoptosis in ischemic human brain endothelium and is neuroprotective. Nat Med 9 (2003) 338-342
38. Hirose K., Okajima K., Taoka Y., et al. Activated protein C reduces the ischemia/reperfusion-induced spinal cord injury in rats by inhibiting neutrophil activation. Ann Surg 232 (2000) 272-280
39. Mizutani A., Okajima K., Uchiba M., and Noguchi T. Activated protein C reduces ischemia/reperfusion induced renal injury in rats by inhibiting leukocyte activation. Blood 95 (2000) 3781-3787
40. Boisclair M.D., Lane D.A., Philippou H., Sheikh S., and Hunt B. Thrombin production, inactivation and expression during open heart surgery measured by assays for activation fragments including a new ELISA for prothrombin fragment F1 + 2. Thromb Haemost 70 (1993) 253-258
41. Brister S.J., Ofosu F.A., and Buchanan M.R. Thrombin generation during cardiac surgery: is heparin the ideal anticoagulant?. Thromb Haemost 70 (1993) 259-262
42. Slaughter T.F., LeBleu T.H., Douglas Jr. J.M., Leslie J.B., Parker J.K., and Greenberg C.S. Characterization of prothrombin activation during cardiac surgery by hemostatic molecular markers. Anesthesiology 80 (1994) 520-526
43. Knudsen L., Hasenkam J.M., Kure H.H., et al. Monitoring thrombin generation with prothrombin fragment 1.2 assay during cardiopulmonary bypass surgery. Thromb Res 84 (1996) 45-54
44. Davies G.C., Sobel M., and Salzman E.W. Elevated plasma fibrinopeptide A and thromboxane B2 levels during cardiopulmonary bypass. Circulation 61 (1980) 808-814
45. Raivio P., Petäjä J., Kuitunen A., and Lassila R. Thrombophilic variables do not increase the generation or procoagulant activity of thrombin during cardiopulmonary bypass. Ann Thorac Surg 85 (2008) 536-542
46. Petäjä J., Pesonen E., Fernandez J.A., Vento A.E., Rämö O.J., and Griffin J.H. Cardiopulmonary bypass and activation of antithrombotic plasma protein C. J Thorac Cardiovasc Surg 118 (1999) 422-429
47. Chandler W.L., and Velan T. Estimating the rate of thrombin and fibrin generation in vivo during cardiopulmonary bypass. Blood 101 (2003) 4355-4362
48. Hattori T., Khan M.M., Colman R.W., and Edmunds Jr. L.H. Plasma tissue factor plus activated peripheral mononuclear cells activate factors VII and X in cardiac surgical wounds. J Am Coll Cardiol 46 (2005) 707-713
49. Kalweit G., Bach J., Huwer H., Winning J., and Hellstern P. The impact of cardiac ischemia and reperfusion on markers of activated haemostasis and fibrinolysis during cardiopulmonary bypass: Comparison of plasma levels in arterial and coronary venous blood. Thromb Res 116 (2005) 33-39
50. Raivio P., Fernandez J.A., Kuitunen A., Griffin J.H., Lassila R., and Petäjä J. Activation of protein C and hemodynamic recovery after coronary artery bypass surgery. J Thorac Cardiovasc Surg 133 (2007) 44-51
51. Clark R.E., Brillman J., Davis D.A., Lovell M.R., Price T.R., and Magovern G.J. Microemboli during coronary artery bypass grafting. Genesis and effect on outcome. J Thorac Cardiovasc Surg 109 (1995) 249-257
52. Dixon B., Santamaria J., and Campbell D. Coagulation activation and organ dysfunction following cardiac surgery. Chest 128 (2005) 229-236
53. Griffin J.H. Blood coagulation: the thrombin paradox. Nature 378 (1995) 337-338
54. Hanson S.R., Griffin J.H., Harker L.A., Kelly A.B., Esmon C.T., and Gruber A. Antithrombotic effects of thrombin-induced activation of endogenous protein C in primates. J Clin Invest 92 (1993) 2003-2012
55. Huntington J.A. Molecular recognition mechanisms of thrombin. J Thromb Haemost 3 (2005) 1861-1872
56. Griffin J.H., Fernandez J.A., Gale A.J., and Mosnier L.O. Activated protein C. J Thromb Haemost 5 Suppl 1 (2007) 73-80
57. Petäjä J., Pesonen E., Fernandez J.A., et al. Activated protein C and inflammation in human myocardium after heart surgery. Am J Hematol 67 (2001) 210-212
58. Sandset P.M., Abildgaard U., and Larsen M.L. Heparin induces release of extrinsic coagulation pathway inhibitor (EPI). Thromb Res 50 (1988) 803-813
59. Adams M.J., Cardigan R.A., Marchant W.A., et al. Tissue factor pathway inhibitor antigen and activity in 96 patients receiving heparin for cardiopulmonary bypass. J Cardiothorac Vasc Anesth 16 (2002) 59-63
60. Donahue B.S., Gailani D., and Mast A.E. Disposition of tissue factor pathway inhibitor during cardiopulmonary bypass. J Thromb Haemost 4 (2006) 1011-1016
61. Kojima T., Gando S., Kemmotsu O., et al. Another point of view on the mechanism of thrombin generation during cardiopulmonary bypass: Role of tissue factor pathway inhibitor. J Cardiothorac Vasc Anesth 15 (2001) 60-64
62. Sun L.B., Utoh J., Kunitomo R., Tsurusaki S., Tagami H., Hirata T., et al. Altered plasma antigen levels of tissue factor pathway inhibitor during open-heart surgery. Surg Today 30 (2000) 122-126
63. Cullmann W., Muller N., Lie T.B., Kladetzky R.G., and Jurgens P. Coagulation parameters and heparin levels in open-heart surgery. Res Exp Med 177 (1980) 111-117
64. Hashimoto K., Yamagishi M., Sasaki T., Nakano M., and Kurosawa H. Heparin and antithrombin III levels during cardiopulmonary bypass: correlation with subclinical plasma coagulation. Ann Thorac Surg 58 (1994) 799-804
65. Ranucci M., Ditta A., Boncilli A., et al. Determinants of antithrombin consumption in cardiac operations requiring cardiopulmonary bypass. Perfusion 19 (2004) 47-52
66. Dietrich W., Spannagl M., Schramm W., Vogt W., Barankay A., and Richter J.A. The influence of preoperative anticoagulation on heparin response during cardiopulmonary bypass. J Thorac Cardiovasc Surg 102 (1991) 505-514
67. Cardigan R.A., Hamilton-Davies C., McDonald S., et al. Haemostatic changes in the pulmonary blood during cardiopulmonary bypass. Blood Coagulation Fibrinolysis 7 (1996) 567-577
68. Brister S.J., and Buchanan M.R. Heparinless cardiopulmonary bypass revisited: A newer strategy to avoid heparin-related bleeding using dermatan sulfate. J Cardiothorac Vasc Anesth 9 (1995) 317-321
69. Mannucci P.M., Tripodi A., Bottasso B., et al. Markers of procoagulant imbalance in patients with inherited thrombophilic syndromes. Thromb Haemost 67 (1992) 200-202
70. Zöller B., Holm J., Svensson P., and Dahlbäck B. Elevated levels of prothrombin activation fragment 1 +2 in plasma from patients with heterozygous Arg506 to Gln mutation in the factor V gene (APC resistance) and/or inherited protein S deficiency. Thromb Haemost 75 (1996) 270-274
71. Gravlee G.P., Haddon W.S., Rothberger H.K., et al. Heparin dosing and monitoring for cardiopulmonary bypass. A comparison of techniques with measurement of subclinical plasma coagulation. J Thorac Cardiovasc Surg 99 (1990) 518-527
72. Okita Y., Takamoto S., Ando M., et al. Coagulation and fibrinolysis system in aortic surgery under deep hypothermic circulatory arrest with aprotinin: The importance of adequate heparinization. Circulation 96 (1997) 376-381
73. Koster A., Fischer T., Praus M., et al. Hemostatic activation and inflammatory response during cardiopulmonary bypass: Impact of heparin management. Anesthesiology 97 (2002) 837-841
74. Despotis G.J., Joist J.H., Hogue Jr. C.W., et al. More effective suppression of hemostatic system activation in patients undergoing cardiac surgery by heparin dosing based on heparin blood concentrations rather than ACT. Thromb Haemost 76 (1996) 902-908
75. Despotis G.J., Joist J.H., Hogue Jr. C.W., et al. The impact of heparin concentration and activated clotting time monitoring on blood conservation. A prospective, randomized evaluation in patients undergoing cardiac operation. J Thorac Cardiovasc Surg 110 (1995) 46-54
76. Raivio P., Kuitunen A., Petäjä J., Ilveskero S., and Lassila R. Monitoring high-dose heparinization during cardiopulmonary by-pass - a comparison between prothrombinase-induced clotting time (PiCT) and two chromogenic anti-factor Xa activity assays. Thromb Haemost 99 (2008) 427-434
77. de Haan J., Boonstra P.W., Monnink S.H., Ebels T., and van Oeveren W. Retransfusion of suctioned blood during cardiopulmonary bypass impairs hemostasis. Ann Thorac Surg 59 (1995) 901-907
78. De Somer F., Van Belleghem Y., Caes F., et al. Tissue factor as the main activator of the coagulation system during cardiopulmonary bypass. J Thorac Cardiovasc Surg 123 (2002) 951-958
79. Aldea G.S., Soltow L.O., Chandler W.L., et al. Limitation of thrombin generation, platelet activation, and inflammation by elimination of cardiotomy suction in patients undergoing coronary artery bypass grafting treated with heparin-bonded circuits. J Thorac Cardiovasc Surg 123 (2002) 742-755
80. Tabuchi N., de Haan J., Boonstra P.W., and van Oeveren W. Activation of fibrinolysis in the pericardial cavity during cardiopulmonary bypass. J Thorac Cardiovasc Surg 106 (1993) 828-833
81. Albes J.M., Stohr I.M., Kaluza M., et al. Physiological coagulation can be maintained in extracorporeal circulation by means of shed blood separation and coating. J Thorac Cardiovasc Surg 126 (2003) 1504-1512
82. Despotis G.J., Gravlee G., Filos K., and Levy J. Anticoagulation monitoring during cardiac surgery: a review of current and emerging techniques. Anesthesiology 91 (1999) 1122-1151
83. Boonstra P.W., Gu Y.J., Akkerman C., Haan J., Huyzen R., and van Oeveren W. Heparin coating of an extracorporeal circuit partly improves hemostasis after cardiopulmonary bypass. J Thorac Cardiovasc Surg 107 (1994) 289-292
84. Gorman R.C., Ziats N., Rao A.K., et al. Surface-bound heparin fails to reduce thrombin formation during clinical cardiopulmonary bypass. J Thorac Cardiovasc Surg 111 (1996) 1-11
85. Muehrcke D.D., McCarthy P.M., Kottke-Marchant K., et al. Biocompatibility of heparin-coated extracorporeal bypass circuits: A randomized, masked clinical trial. J Thorac Cardiovasc Surg 112 (1996) 472-483
86. Ovrum E., Brosstad F., Am Holen E., Tangen G., and Abdelnoor M. Effects on coagulation and fibrinolysis with reduced versus full systemic heparinization and heparin-coated cardiopulmonary bypass. Circulation 92 (1995) 2579-2584
87. Wagner W.R., Johnson P.C., Thompson K.A., and Marrone G.C. Heparin-coated cardiopulmonary bypass circuits: Hemostatic alterations and postoperative blood loss. Ann Thorac Surg 58 (1994) 734-740
88. te Velthuis H., Baufreton C., Jansen P.G., et al. Heparin coating of extracorporeal circuits inhibits contact activation during cardiac operations. J Thorac Cardiovasc Surg 114 (1997) 117-122
89. Gu Y.J., van Oeveren W., van der Kamp K.W., Akkerman C., Boonstra P.W., and Wildevuur C.R. Heparin coating of extracorporeal circuits reduces thrombin formation in patients undergoing cardiopulmonary bypass. Perfusion 6 (1991) 221-225
90. Aldea G.S., O'Gara P., Shapira O.M., et al. Effect of anticoagulation protocol on outcome in patients undergoing CABG with heparin-bonded cardiopulmonary bypass circuits. Ann Thorac Surg 65 (1998) 425-433
91. Kuitunen A.H., Heikkilä L.J., and Salmenperä M.T. Cardiopulmonary bypass with heparin-coated circuits and reduced systemic anticoagulation. Ann Thorac Surg 63 (1997) 438-444
92. Ovrum E., Brosstad F., Am Holen E., Tangen G., Abdelnoor M., and Oystese R. Complete heparin-coated (CBAS) cardiopulmonary bypass and reduced systemic heparin dose; effects on coagulation and fibrinolysis. Eur J Cardio-Thorac Surg 10 (1996) 449-455
93. Koster A., Yeter R., Buz S., et al. Assessment of hemostatic activation during cardiopulmonary bypass for coronary artery bypass grafting with bivalirudin: Results of a pilot study. J Thorac Cardiovasc Surg 129 (2005) 1391-1394