Skip to main content
Log in

The Role of Coagulation in Systemic Inflammation: A Review of the Experimental Evidence

  • Published:
Sepsis

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

References

  1. Greenman RL, Schein RM, Martin MA, et al. A controlled clinical trial of E5 murine monoclonal IgM antibody to endotoxin in the treatment of gram-negative sepsis. The XOMA Sepsis Study Group, JAMA 1991; 266:1097-1102.

    PubMed  Google Scholar 

  2. McCloskey RV, Straube RC, Sanders C, Smith SM, Smith CR. Treatment of septic shock with human monoclonal antibody HA-1A. A randomized, double-blind, placebo-controlled trial. CHESS Trial Study Group. Ann Intern Med 1994; 121:1-5 (1994)

    PubMed  Google Scholar 

  3. Abraham E, Anzueto A, Gutierrez G, et al. Double-blind randomised clinical trial of monoclonal antibody to human tumour necrosis factor in treatment of septic shock. NORASEPT II Study Group, Lancet 1998;351:929-933.

    PubMed  Google Scholar 

  4. Abraham E, Glauser MP, Butler T, et al. p55 Tumour necrosis factor receptor fusion protein in the treatment of patients with severe sepsis and septic shock. A randomized controlled multicenter trial. Ro 45-2081 Study Group, 1997; JAMA 277:1531-1538.

    PubMed  Google Scholar 

  5. Fisher CJ, Dhainaut J-FA, Opal SM, et al. Recombinant human Interleukin1 receptor antagonist in the treatment of patients with the sepsis syndrome. JAMA 1994;271:1836-1843.

    PubMed  Google Scholar 

  6. Pinner RW, Teutsch SM, Simonsen L, et al. Trends in infectious diseases mortality in the United States. 1996; JAMA 275:189-193.

    PubMed  Google Scholar 

  7. Cohen ML. Epidemiology of drug resistance: Implications for a post-antimicrobial era, Science 1992;257:1050-1055.

    PubMed  Google Scholar 

  8. Kingman S. Resistance a European problem, too. Science 1994;264:363-364.

    PubMed  Google Scholar 

  9. Casadevall A. Crisis in infectious diseases: Time for a new paradigm? Clin Infect Dis 1996;23:790:794.

    PubMed  Google Scholar 

  10. Fourrier F, Chopin C, Goudemand J, et al. Septic shock, multiple organ failure and DIC: Compared patterns of antithrombin III, protein C, and protein S deficiencies. Chest 1992;101:816-823.

    PubMed  Google Scholar 

  11. Rangel-Frausto MS, Pittet D, Costigan M, Hwang T, Davis CS, Wenzel RP. The natural history of the systemic inflammatory response syndrome (SIRS). JAMA 1995;273:117-123.

    PubMed  Google Scholar 

  12. Voss R, Matthias FR, Borkowski G, Reitz D. Activation and inhibition of fibrinolysis in septic patients in an internal intensive care unit. Br J Haem 1990;75:99-105.

    Google Scholar 

  13. Brisseau GF, Cheung PC, Rotstein OD. The role of macrophage procoagulants in infection. In: Levy G.A., Cole E. eds. Procoagulant Activity in Health and Disease CRC Press, Boca Raton 1993:69-85.

    Google Scholar 

  14. Taylor FB Jr. The inflammatory-coagulant axis in the host response to gram-negative sepsis: Regulatory roles of proteins and inhibitors of tissue factor. New Horizons 1994;2:555-565.

    PubMed  Google Scholar 

  15. Drake TA, Cheng J, Chang A, Taylor FB Jr. Expression of tissue factor, thrombomodulin, and E-selectin in baboons with lethal Escherichia coli sepsis. Am J Path 1993;142:1458-1470.

    PubMed  Google Scholar 

  16. Mackman N, Sawdey MS, Keeton MR, Loskutoff DJ. Murine tissue factor gene expression in vivo; Tissue and cell specificity and regulation by lipopolysaccharide. Am J Path 1993; 143:76-84.

    PubMed  Google Scholar 

  17. Osterud B, Flaegstad T. Increased tissue thromboplastin activity in monocytes of patients with meningococcal infection: Related to an unfavourable prognosis. Thromb Hemost 1983;49:5-7.

    Google Scholar 

  18. Wolbink GJ, Bossink AW, Groeneveld AB, de Groot MC, Thijs LG, Hack CE. Complement activation in patients with sepsis is in part mediated by C-reactive protein. J Infect Dis 1998;177:81-7.

    PubMed  Google Scholar 

  19. Lin RY, Astiz ME, Saxon JC, Saha DC, Rackow EC. Relationships between plasma cytokine concentrations and leukocyte functional antigen expression in patients with sepsis. Crit Care Med 1994;22:1595-1602.

    PubMed  Google Scholar 

  20. Carson SD, Johnson DR. Consecutive enzyme cascades: Complement activation at the cell surface triggers increased tissue factor activity. Blood 1990;76:361-367.

    PubMed  Google Scholar 

  21. Wiedmer T, Esmon CT Sims PJ. Complement proteins C5b-9 stimulate procoagulant activity through platelet prothrombinase. Blood 1986;68:875-880.

    PubMed  Google Scholar 

  22. Sims PJ, Faioni EM, Wiedmer T, Shattil SJ. Complement proteins C5b-9 cause release of membrane vesicle from the platelet surface that are enriched in the membrane receptor for coagulation Factor Va and express prothrombinase activity, J Biol Chem 1988;263:18205-18212.

    PubMed  Google Scholar 

  23. Altieri DC, Morrissey JH, Edgington TS. Adhesive receptor Mac-1 coordinates the activation of factor X on stimulated cells of monocytic and myeloid differentiation: an alternative initiation of the coagulation protease cascade. PNASUSA 1988;85:7462-7466.

    Google Scholar 

  24. McGilvray ID, Lu Z, Wei AC, Rostein OD. MAP-Kinase dependent induction of monocytic procoagulant activity by β2-integrins. J Surg Res 1998 (in press).

  25. Fan ST, Edgington TS. Integrin regulation of leukocyte inflammatory functions: CD11b/CD18 enhancement of the TNFα responses of monocytes. J Immunol 1993;150:2972.

    PubMed  Google Scholar 

  26. Altieri DC. Coagulation assembly on leukocytes in transmembrane signaling and cell adhesion. Blood 1993;81:569-579.

    PubMed  Google Scholar 

  27. Kaminishi H, Hamatake H, Cho T, et al. Activation of blood clotting factors by microbial proteinase. FEMS Micro Letters 1994;121:327-332.

    Google Scholar 

  28. Kalter ES, Daha MR, ten Cate JW, et al. Activation and inhibition of Hageman factor-dependent pathways and the complement system in uncomplicated bacteremia or bacterial shock. J Infect Dis 1985;151:1019-1027.

    PubMed  Google Scholar 

  29. Jesty J, Lorenz A, Rodriduez J, Wun T-C. Initiation of the tissue factor pathway of coagulation in the presence of heparin: control by antithrombin III and tissue factor pathway inhibitor. Blood 1996;87:2301-2307.

    PubMed  Google Scholar 

  30. McVey JH. Tissue Factor Pathway. Bailliere's Clinical Haematology 1994;7:469-484.

    PubMed  Google Scholar 

  31. Sakata Y, Loskutoff DJ, Gladson C L, et al. Mechanism of protein C-dependent clot lysis: Role of plasminogen activator inhibitor. Blood 1986;68:1218-1223.

    PubMed  Google Scholar 

  32. Meesters RM, Mannucci PM, Coppola R, et al. Factor VIIa and Antithrombin III activity during severe sepsis and septic shock in neutropenic patients. Blood 1996;88:881-886.

    PubMed  Google Scholar 

  33. Thijs LG, de Boer JP, de Groot MCM, Hack CE. Coagulation disorders in septic shock. Intensive Care Med 1993; 19:s8-15.

    PubMed  Google Scholar 

  34. Alcaraz A, Espana F, Sanchez-Cuenca J, et al. Activation of the protein C pathway in acute sepsis, Thromb Res 1995; 79:83-93.

    PubMed  Google Scholar 

  35. Hesselvik JF, Malm J, Dahlback B, et al. Protein C, Protein S and C4b-binding protein in severe infection and septic shock. Thromb Hemost 1991;65:126-129.

    Google Scholar 

  36. Nawroth PP, Stern DM. Modulation of endothelial cell hemostatic properties by tumor necrosis factor. J Exp Med 1986; 163:740-745.

    PubMed  Google Scholar 

  37. Fourrier F, Jourdain M, Tournois A, Caron C, Goudemand J, Chopin C. Coagulation inhibitor substitution during sepsis. Intensive Care Med 1995;21:s264-268.

    PubMed  Google Scholar 

  38. Boldt J, Heesen M, Welters I, Padberg W, Martin K, Hempelmann G. Does the type of volume therapy influence endothelial-relate coagulation in the critically ill? Br J Anaesth 1995;75:740-746.

    PubMed  Google Scholar 

  39. Carr C, Bild GS, Chang AC, et al. Recombinant E. Coli-derived tissue factor pathway inhibitor reduces coagulopathic and lethal effects in the baboon gram-negative model of septic shock. Circ Shock 1994;44:126-137.

    PubMed  Google Scholar 

  40. Creasey AA, Chang ACK, Feigen L, Wun T-C, Taylor FB Jr., Hinshaw LB. Tissue Factor Pathway Inhibitor Reduces Mortality from Escherichia coli Septic Shock. J Clin Invest 1993;91:2850-2860.

    PubMed  Google Scholar 

  41. Pralong G, Calandra T, Glauser MP, et al. Plasminogen Activator Inhibitor-1: A New prognostic marker in septic shock. Thromb Hemost 1989;61:459-462.

    Google Scholar 

  42. Suffredini AF, Harpel PC, Parrillo JE. Promotion and subsequent inhibition of plasminogen activation after administration of intravenous endotoxin to normal subjects. NEJM 1989;320:1165-1172.

    PubMed  Google Scholar 

  43. Schuster HP. ATIII in septicemia with DIC. Intensive Care Med 1993;19:s16-18.

    PubMed  Google Scholar 

  44. Mammen EF, Miyakawa T, Phillips TF, Assarian GS, Brown JM, Murano G. Human antithrombin concentrates and experimental disseminated intravascular coagulation. Sem Thromb Hemost 1985:11:373-383.

    Google Scholar 

  45. Hesselvik JF, Blomback M, Brodin B, Maller R. Coagulation, fibrinolysis, and kallikrein systems in sepsis: Relation to outcome. Crit Care Med 1989;17:724-733.

    PubMed  Google Scholar 

  46. Bick, RL. Disseminated Intravascular Coagulation. Hem/Onc Clin of North Am 1992;6(6):1259-1285.

    Google Scholar 

  47. Carrico CJ, Meakins JL, Marshall JC, Fry D, Maier RV. Multiple-organ-failure syndrome. Arch Surg 1986;121:196.

    PubMed  Google Scholar 

  48. Schlag G, Redl H. Morphology of the microvascular system in shock: lung, liver and skeletal muscles, Crit Care Med 1985;13:1045.

    PubMed  Google Scholar 

  49. Shibayama Y. Sinusoidal circulatory disturbance by micro-thrombosis as a cause of endotoxin-induced hepatic injury. J Pathol 1987;151:315.

    PubMed  Google Scholar 

  50. Bar-Shavit R, Kahn A, Mudd MS, Wilner GD, Mann KG, Fenton JW. Localization of a chemotactic domain in human thrombin. Biochem 1985;23:397-400.

    Google Scholar 

  51. Bar-Shavit R, Kahn A, Wilner GD. Monocyte chemotaxis: Stimulation by specific exosite region in thrombin. Science 1983;220:728-731.

    PubMed  Google Scholar 

  52. Ferrara JJ, Kan C, Luterman A, Curreri PW. Effects of fibrinogen degradation fragments D and E on cell-mediated immunity. J Surg Res 1989;47:134.

    PubMed  Google Scholar 

  53. Senior RM, Skogen WF, Griffen GL, Wilner GD, Effects of fibrinogen derivatives upon the inflammatory response. J Clin Invest 1986;77:1014.

    PubMed  Google Scholar 

  54. Stecher VJ, Sorkin E. The chemotactic activity of fibrin lysis products, Int Arch Allerg Appl Immunol 1972;43:879.

    Google Scholar 

  55. Cirino G, Cicala C, Bucci MR, Sorrentino L, Maraganore JM, Stone SR. Thrombin as an inflammatory mediator through activation of its receptor. J Exp Med 1996;83:821-827.

    Google Scholar 

  56. Cirino G, Cicala C, Bucci M, et al. Factor Xa as an interface between coagulation and inflammation. Molecular mimicry of Factor Xa association with effector cell protease receptor-1 induces acute inflammation in vivo. J Clin Invest 1997;99: 2446-2451 (1997)

    PubMed  Google Scholar 

  57. Strukova SM, Dugina TN, Khgatian SV, Redkozubov AE, Redkozuba GP, Pinelis VG. Thrombin-mediated events implicated in mast cell activation, Sem Thromb Hemost 1996; 22:145-150.

    Google Scholar 

  58. McGilvray ID, Rotstein OD. The role of procoagulants in the local and systemic inflammatory response, World Journal of Surgery 1998;22:179-186.

    PubMed  Google Scholar 

  59. Dunn DL, Simmons RL. Fibrin in peritonitis III. The mechanism of bacterial trapping by polymerizing firin. Surgery 1982;92:513.

    PubMed  Google Scholar 

  60. Zinsser HH, Pryde AW. Experimental study of physical factors, including fibrin formation, influencing the spread of fluids and small particles within and from the peritoneal cavity of a dog. Ann Surg 1952;136:818.

    PubMed  Google Scholar 

  61. Ciano PS, Colvin RB, Dvorak AM, Mcdonagh J, Dvorak HF. Macrophage migration in fibin gel matrice. Lab Invest 1986; 54:62.

    PubMed  Google Scholar 

  62. Kazura JW, Wenger JD, Salata RA, Budzynski AZ, Goldsmith GH. Modulation of polymorphonuclear leukocyte microbicidal activity and oxidative metabolism by fibrinogen degradation products D and E. J Clin Invest 1989;83:1916.

    PubMed  Google Scholar 

  63. Rotstein OD, Pruett TL, Simmons RL. Fibrin in peritonits V. Fibrin inhibits phagocytic killing of Escherichia coli by human polymorphonuclear leukocytes. Ann Surg 1986;203: 413.

    PubMed  Google Scholar 

  64. van Deventer SJH, Buller HR, ten Cate JW, Aarden LA, Hack CE, Sturk A. Experimental endotoxemia in humans: Analysis of cytokine release and coagulation, fibrinolytic and complement pathways. Blood 1990;76:2520-2526.

    PubMed  Google Scholar 

  65. van der Poll T, Buller HR, ten Cate H, et al. Activation of coagulation after administration of tumour necrosis factor to normal subjects. NEJM 1990;322:1622-1627.

    PubMed  Google Scholar 

  66. van der Poll T, Levi M, Buller HR, et al. Fibrinolytic response to tumour necrosis factor in healthy subjects. J Exp Med 1991;174:729-732.

    PubMed  Google Scholar 

  67. Inoue Y, Kohno S, Miyazaki T, Yamaguchi K. Effect of a platelet activating factor antagonist and antithrombin III on septicemia and endotoxemia in rats. Tohoku J Exp Med 1991; 163:175-185.

    PubMed  Google Scholar 

  68. Emerson TE, Fournel MA, Redens TB, Taylor FB. Efficacy of antithrombin III supplementation in animal models of fulminant Escherichia coli endotoxemia or bacteremia, Am J Med 1989;87(3B):27s-33s.

    PubMed  Google Scholar 

  69. Redens TB, Emerson TE. Antithrombin-III treatment limits disseminated intravascular coagulation in endotoxemia. Circ Shock 1989;28:49-58.

    PubMed  Google Scholar 

  70. Spannagl M, Hoffman H, Sieback M, Weipert J, Schwarz HP, Schramm W. A purified antithrombin III-heparin complex as a potent inhibitor of thrombin in porcine endotoxin shock. Thromb Res 1991;61:1-10.

    PubMed  Google Scholar 

  71. Hardaway RM, Hasni EA, Eseever EF. Endotoxin shock, a manifestation of intravascular coagulation. Ann Surg 1961; 154:791-802.

    PubMed  Google Scholar 

  72. Hardaway RM, Johnson D. A unified theory of shock. Am Surg 1963:292-298.

  73. Margaretten W, McKay DG, Phillips LL. The effect of heparin on endotoxin shock in the rat. Am J Path 1967;51:61-68.

    Google Scholar 

  74. Filkins JP, DiLuzio NR. Heparin protection in endotoxin shock. Am J Physiol 1968;214:1074-1077.

    PubMed  Google Scholar 

  75. Feinstein DL. Diagnosis and Management of DIC: The Role of Heparin Therapy. Blood 1982;60:284-287.

    PubMed  Google Scholar 

  76. Hardaway RM, Williams CH, Sun Y. A new approach to the treatment of experimental septic shock. J Surg Res 1996; 61:311-316 (1996)

    PubMed  Google Scholar 

  77. Wuillemin WA, te Velthuis H, Lubbers YT, de Ruig CP, Eldering E, Hack CE. Potentiation of C1 inhibitor by glycosaminoglycans: dextran sulfate species are effective inhibitors of in vitro complement activation in plasma. J Immunol 1997;159:1953-1960.

    PubMed  Google Scholar 

  78. Gralinsky MR, Park JL, Ozeck MA, Wiater BC, Lucchesi BR. LU 51198, a highly sulfated, low-molecular weight heparin derivative, prevents complement-mediated myocardial injury in the perfused rabbit heart. J Pharmacol Exp Ther 1997;282:554-560.

    PubMed  Google Scholar 

  79. Chalkiadakis G, Kostakis A, Karayannacos PE, et al. The effect of heparin upon fibrinopurulent peritonits in rats. Surg Gynecol Obstet 1983;157:257.

    PubMed  Google Scholar 

  80. Davidson R K, Cardenas A, Busuttil R W. The effects of heparin and low molecular weight dextran on survival after fibrinopurulent peritonitis. Surg Gynecol Obstet 1981;153:327.

    PubMed  Google Scholar 

  81. Gaskins RA, Dalidorf FG. Experimental meningococcal septicemia: Effect of heparin therapy. Arch Path Lab Med 1976;100:318-324.

    PubMed  Google Scholar 

  82. Dickneite G, Czech J. Combination of antibiotic treatment with the thrombin inhibitor recombinant hirudin for the therapy of experimental Klebsiella pneumoniae sepsis. Thromb Hemost 1994;71:768-772.

    Google Scholar 

  83. Dunn DL, Mach PA, Cerra FB, Ferguson RM. The role of heparin in guinea pig gram negative bacterial sepsis. J Surg Res 1983;34:479-485.

    PubMed  Google Scholar 

  84. Corrigan JJ, Kiernat JF. Effect of heparin in experimental gram-negative septicemia. J Infect Dis 1975;131:138-143.

    PubMed  Google Scholar 

  85. Taylor FB Jr, Chang A, Esmon CT, D'Angelo A, Vigano-D'Angelo S, Blick K E. Protein C prevents the coagulopathic and lethal effects of Escherichia coli infusion in the baboon. J Clin Invest 1987;79:918-925.

    PubMed  Google Scholar 

  86. Taylor FB, Chang A, Ferrell G, et al. C4b-Binding protein exacerbates the host response to Escherichia coli. Blood 1991;78:357-363.

    PubMed  Google Scholar 

  87. Murakami K, Okajima K, Uchiba M, et al. Activated protein C attenuates endotoxin-induced pulmonary vascular injury by inhibiting activated leukocytes in rats. Blood 1996;87: 642-647.

    PubMed  Google Scholar 

  88. Taylor FB, Chang ACK, Peer TK, et al. CT, DEGR-Factor Xa blocks disseminated intravascular coagulation initiated by Escherichia coli without preventing shock or organ damage. Blood 1991;78:364-368.

    PubMed  Google Scholar 

  89. Taylor FB, Hoogendoorn H, Chang ACK, et al. Anticoagulant and fibrinolytic activities are promoted, not retarded, in vivo after thrombin generation in the presence of a monoclonal antibody that inhibits activation of protein C. Blood 1992;79:1720-1728.

    PubMed  Google Scholar 

  90. Hardaway RM, Williams CH. Prevention of multiple organ failure with plasminogen activator. Curr Ther Res 1991;49: 711-722.

    Google Scholar 

  91. Hardaway RM, Williams CH, Marvasti M. Prevention of adult respiratory distress syndrome with plasminogen activator in pigs. Crit Care Med 1990;18:1413-1418.

    PubMed  Google Scholar 

  92. Smith EF, Kinter LB, Jugus M, Zeid R. Effect of the thrombolytic agent, streptokinase, on the responses to endotoxemia in conscious rats. Circ Shock 1988;25:85-94.

    PubMed  Google Scholar 

  93. Rotstein OD, Kao J. Prevention of intra-abdominal abscesses by fibrinolysis using recombinant tissue plasminogen activator. J Infect Dis 1988;158:766-772.

    PubMed  Google Scholar 

  94. McRitchie DI, Girotti MJ, Glynn MF, Goldberg JM, Rotstein OD. Effect of systemic fibrinogen depletion on intraabdominal abscess formation. J Lab Clin Med 1991;118:48.

    PubMed  Google Scholar 

  95. Zenz W, Muntean W, Zobel G, Grubauer HK, Gallistl S. Treatment of fulminant meningococcemia with recombinant Tissue Plasminogen Activator. Thromb Hemost 1995;74:802-803.

    Google Scholar 

  96. Bone RC. Modulators of coagulation: A Critical appraisal of their role in sepsis. Arch Int Med 1992;152:1381-1389.

    Google Scholar 

  97. Pixley RA, DeLa Cadena RA, Page JD, et al. Activation of the contact system in lethal hypotensive bacteremia in a baboon model. Am J Path 1992;140:897-906.

    PubMed  Google Scholar 

  98. Pixley RA, de la Cadena R, Page JD, et al. The contact system contributes to hypotension but not disseminated intravascular coagulation in lethal bacteremia. J Clin Invest 1993;91:61-68.

    PubMed  Google Scholar 

  99. Kaufman N, Page JD, Pixley RA, Schein R, Schmaier AH, Colman R.W. α2-Macroglobulin-kallikrein complexes detect contact system activation in hereditary angioedema and human sepsis. Blood 1991;77:2660-2667.

    PubMed  Google Scholar 

  100. Fischer MB, Prodeus AP, Nicholson-Weller A, et al. Increased susceptibility to endotoxin shock in complement C3-and C4-deficient mice is corrected by C1 inhibitor replacement. J Immunol 1997;159:976-82.

    PubMed  Google Scholar 

  101. Hack CE, Voerman HJ, Eisele B, et al. C1-Esterase inhibitor substitution in sepsis. Lancet 1992;339:378.

    PubMed  Google Scholar 

  102. Hack CE, Ogilvie AC, Eisele B, Eerenberg AJM, Wagstaff J, Thijs LG. C1-Inhibitor substitution therapy in septic shock and in the vascular leak syndrome induced by high doses of interleukin-2. Intensive Care Med 1993;19:s19-s28.

    PubMed  Google Scholar 

  103. Hack CE, Ogilvie AC, Eisele B, Jansen PM, Wagstaff J, Thijs LG. Initial studies on the administration of C1-esterase inhibitor to patients with septic shock or with a vascular leak syndrome induced by interleukin-2 therapy. Prog Clin Biol Res 1994;388:335-357.

    PubMed  Google Scholar 

  104. Dackiw AP, McGilvray ID, Woodside M, Nathens AB, Marshall JC, Rotstein OD. Prevention of endotoxin-induced mortality by anti-tissue factor immunization. Arch Surg 1996;131:1273-8.

    PubMed  Google Scholar 

  105. Biemond BJ, Levi M, ten Cate H, et al. Complete inhibition of endotoxin-induced coagulation activation in chimpanzees with a monoclonal Fab fragment against factor VII/VIIa. Thromb Hemost 1995;73:223-230.

    Google Scholar 

  106. Levi M, ten Cate H, Bauer KA, et al. Inhibition of endotoxin-induced activation of coagulation and fibrinolysis by pentoxifylline or by a monoclonal anti-tissue factor antibody in chimpanzees. J Clin Invest 1994;93:114-20.

    PubMed  Google Scholar 

  107. Day KC, Hoffman LC, Palmier MO, et al. Recombinant lipotprotein-associated coagulation inhibitor inhibits tissue thromboplastin-induced intravascular coagulation in the rabbit. Blood 1990;76:1538-45.

    PubMed  Google Scholar 

  108. Taylor FB, Chang A, Ruf W, et al. Lethal E Coli septic shock is prevented by blocking tissue factor with monoclonal antibody. Circ Shock 1991;33:127-34.

    PubMed  Google Scholar 

  109. Warr TA, Rao VM, Rapaport SI. Disseminated intravascular coagulation in rabbits induced by administration of endotoxin or tissue factor: Effect of anti-tissue factor antibodies and measurement of plasma extrinsic pathway inhibitor activity. Blood 1990;75:1481-89.

    PubMed  Google Scholar 

  110. Gomez C, Paramo JA, Rocha E. Effect of heparin and/or antithrombin III in a model of disseminated intravascular coagulation induced by endotoxin in rabbits. Sangre 1992; 37:5-10.

    PubMed  Google Scholar 

  111. McRitchie DI, Cummings D, Rotstein OD. Delayed administration of tissue plasminogen activator reduces intra-abdominal abscess formation. Arch Surg 1989;124:1406-1410.

    PubMed  Google Scholar 

  112. Rosenthal GA, Qunto J, Kao J, Rostein OD, Prevention of intra-abdominal abscesses with fibrinolytic agents. Can J Surg 1988;31:98-100.

    PubMed  Google Scholar 

  113. Houston KA, McRitchie DI, Rotstein OD. Tissue plasmingen activator reverses the deleterious effect of infection on colonic wound healing. Ann Surg 1990;211:130-135.

    PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

McGilvray, I.D., Rotstein, O.D. The Role of Coagulation in Systemic Inflammation: A Review of the Experimental Evidence. Sepsis 2, 199–208 (1998). https://doi.org/10.1023/A:1009825611729

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1009825611729

Keywords

Navigation