New insights into pathways that determine the link between infection and thrombosis

Netherlands Journal of Medicine

Volumn 70, Issue 3, 2012, Pages 114-120

  Levi, M ^a   van der Poll, T ^a   Schultz, M ^a  

^a UNIVERSITY OF AMSTERDAM   (Netherlands)

Author keywords

Coagulation; Cytokines; Endothelium; Infection; Inflammation; Thrombosis

Indexed keywords

ANTICOAGULANT AGENT; ANTITHROMBIN; BLOOD CLOTTING FACTOR 10; BLOOD CLOTTING FACTOR 10A; BLOOD CLOTTING FACTOR 7A; BLOOD CLOTTING FACTOR 9; FIBRIN; HEPARIN; INTERLEUKIN 6; PROTEIN C; RECOMBINANT NEMATODE ANTICOAGULANT PROTEIN C2; RECOMBINANT PROTEIN; RECOMBINANT THROMBOMODULIN; RECOMBINANT TISSUE FACTOR PATHWAY INHIBITOR; THROMBOPLASTIN; TISSUE FACTOR PATHWAY INHIBITOR; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ANTICOAGULANT THERAPY; BLOOD CLOTTING; CYTOMEGALOVIRUS INFECTION; DISEASE ASSOCIATION; DISSEMINATED INTRAVASCULAR CLOTTING; DRUG SAFETY; ENDOTHELIUM CELL; FIBRIN FORMATION; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; INFECTION; INFLAMMATION; LOW DRUG DOSE; LUNG EMBOLISM; NONHUMAN; PROTEIN BLOOD LEVEL; PROTEIN EXPRESSION; REVIEW; SEPSIS; SYSTEMIC INFLAMMATORY RESPONSE SYNDROME; THROMBOCYTE ACTIVATION; THROMBOEMBOLISM; THROMBOGENESIS; THROMBOSIS; VASCULAR DISEASE; VASCULAR ENDOTHELIUM; VASCULITIS;

BLOOD COAGULATION; CYTOKINES; ENDOTHELIUM, VASCULAR; FIBRINOLYSIS; HEMOSTASIS; HUMANS; INFECTION; THROMBOSIS;

EID: 84860185870     PISSN: 03002977     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Review

References (106)

1. Levi M, ten Cate H. Disseminated intravascular coagulation. N Engl J Med. 1999;341:586-592.
2. Wheeler AP, Bernard GR. Treating patients with severe sepsis. N Engl J Med. 1999;340:207-214.
3. Levi M, Keller TT, van Gorp E, ten Cate H. Infection and inflammation and the coagulation system. Cardiovasc Res. 2003;60:26-39.
4. Levi M, Schultsz M, van der Poll T. Infection and inflammation as a risk factor for thrombosis. Sem Thromb Hemostas. 2012; in press.
5. Levi M, van der Poll T. Inflammation and coagulation. Crit Care Med. 2010;38:S26-S34.
6. Esmon CT, Fukudome K, Mather T, et al. Inflammation, sepsis, and coagulation. Haematologica. 1999;84:254-259.
7. Levi M, van der Poll T, ten Cate H, van Deventer SJ. The cytokine-mediated imbalance between coagulant and anticoagulant mechanisms in sepsis and endotoxaemia. Eur J Clin Invest. 1997;27:3-9.
8. Osterud B, Bjorklid E. The tissue factor pathway in disseminated intravascular coagulation. Semin Thromb Hemost. 2001;27:605-617.
9. Taylor FB. Response of anticoagulant pathways in disseminated intravascular coagulation. Semin Thromb Hemost. 2001;27:619631.
10. ten Cate JW, van der Poll T, Levi M, et al. Cytokines: triggers of clinical thrombotic disease. Thromb Haemost. 1997;78:415-419.
11. Aird WC. Vascular bed-specific hemostasis: role of endothelium in sepsis pathogenesis. Crit Care Med. 2001;29:S28-S34.
12. Levi M, ten Cate H, van der Poll T. Endothelium: interface between coagulation and infammation. Crit Care Med. 2002;30:S220-S224.
13. Vallet B. Microthrombosis in sepsis. Minerva Anestesiol. 2001;67:298-301.
14. Levi M, van der Poll T, ten Cate H. Tissue factor in infection and severe inflammation. Semin Thromb Hemost. 2006;32:33-39.
15. Taylor FBJ, Chang A, Ruf W, et al. Lethal E. coli septic shock is prevented by blocking tissue factor with monoclonal antibody. Circ Shock. 1991;33:127-134.
16. 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;93:114-120.
17. van der Poll T, Levi M, Hack CE, et al. Elimination of interleukin 6 attenuates coagulation activation in experimental endotoxemia in chimpanzees. J Exp Med. 1994;179:1253-1259.
18. Libby P, Aikawa M. Stabilization of atherosclerotic plaques: new mechanisms and clinical targets. Nat Med. 2002;8:1257-1262.
19. Osterud B, Rao LV, Olsen JO. Induction of tissue factor expression in whole blood - lack of evidence for the presence of tissue factor expression on granulocytes. Thromb Haemost. 2000;83:861-7.
20. Franco RF, de Jonge E, Dekkers PE, et al. The in vivo kinetics of tissue factor messenger RNA expression during human endotoxemia: relationship with activation of coagulation. Blood. 2000;96:554-559.
21. Rauch U, Bonderman D, Bohrmann B, et al. Transfer of tissue factor from leukocytes to platelets is mediated by CD15 and tissue factor. Blood. 2000;96:170-175.
22. Osterud B, Bjorklid E. Sources of tissue factor. Semin Thromb Hemost. 2006;32:11-23.
23. Lowenberg EC, Meijers JC, Levi M. Platelet-vessel wall interaction in health and disease. Neth J Med. 2010;68:242-251.
24. Osterud B. Tissue factor expression by monocytes: regulation and pathophysiological roles. Blood Coagul Fibrinolysis. 1998;9 Suppl 1:S9-S14.
25. Furie B, Furie BC. Role of platelet P-selectin and microparticle PSGL-1 in thrombus formation. Trends Mol Med. 2004;10:171-178.
26. Neumann FJ, Marx N, Gawaz M, et al. Induction of cytokine expression in leukocytes by binding of thrombin-stimulated platelets. Circulation. 1997;95:2387-2394.
27. Levi M, van der Poll T. The role of natural anticoagulants in the pathogenesis and management of systemic activation of coagulation and infammation in critically ill patients. Semin Thromb Hemost. 2008;34:459-468.
28. Levi M. Antithrombin in sepsis revisited. Crit Care. 2005;9:624-625.
29. Levi M, van der Poll T, Buller HR. Bidirectional relation between inflammation and coagulation. Circulation. 2004;109:2698-2704.
30. Kobayashi M, Shimada K, Ozawa T. Human recombinant interleukin-1 beta- and tumor necrosis factor alpha-mediated suppression of heparin-like compounds on cultured porcine aortic endothelial cells. J Cell Physiol. 1990;144:383-390.
31. Levi M, van der Poll T. Recombinant human activated protein C: current insights into its mechanism of action. Crit Care. 2007;11 Suppl 5:S3:S3.
32. Esmon CT. Role of coagulation inhibitors in infammation. Thromb Haemost. 2001;86:51-56.
33. Levi M, de Jonge E, van der Poll T. Rationale for restoration of physiological anticoagulant pathways in patients with sepsis and disseminated intravascular coagulation. Crit Care Med. 2001;29:S90-S94.
34. Esmon CT. The regulation of natural anticoagulant pathways. Science. 1987;235:1348-1352.
35. Esmon C T. The endothelial cell protein C receptor [Review.] Thromb Haemost. 2000;83:639-643.
36. Perez-Casal M, Downey C, Fukudome K, Marx G, Toh CH. Activated protein C induces the release of microparticle-associated endothelial protein C receptor. Blood. 2005;105:1515-1522.
37. Mesters RM, Helterbrand J, Utterback BG, et al. Prognostic value of protein C concentrations in neutropenic patients at high risk of severe septic complications. Crit Care Med. 2000;28:2209-2216.
38. Vary TC, Kimball SR. Regulation of hepatic protein synthesis in chronic inflammation and sepsis. Am J Physiol. 1992;262:C445-C452.
39. Eckle I, Seitz R, Egbring R, Kolb G, Havemann K. Protein C degradation in vitro by neutrophil elastase. Biol Chem Hoppe Seyler. 1991;372:1007-1013.
40. Nawroth PP, Stern DM. Modulation of endothelial cell hemostatic properties by tumor necrosis factor. J Exp Med. 1986;163:740-745.
41. Faust SN, Levin M, Harrison OB, et al. Dysfunction of endothelial protein C activation in severe meningococcal sepsis. N Engl J Med. 2001;345:408-416.
42. Garcia de Frutos P, Alim RI, Hardig Y, et al. Differential regulation of alpha and beta chains of C4b-binding protein during acute-phase response resulting in stable plasma levels of free anticoagulant protein S. Blood. 1994;84:815-822.
43. Taylor FBJ, Dahlback B, Chang AC, et al. Role of free protein S and C4b binding protein in regulating the coagulant response to Escherichia coli. Blood. 1995;86:2642-2652.
44. Taylor FBJ, Stearns-Kurosawa DJ, Kurosawa S, et al. The endothelial cell protein C receptor aids in host defense against Escherichia coli sepsis. Blood. 2000;95:1680-1686.
45. De Pont AC, Bakhtiari K, Hutten BA, et al. Endotoxaemia induces resistance to activated protein C in healthy humans. Br J Haematol. 2006;134:213-219.
46. Biemond BJ, 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 (Colch). 1995;88:587-594.
47. Biemond BJ, Friederich PW, Koschinsky ML, et al. Apolipoprotein(a) attenuates endogenous fibrinolysis in the rabbit jugular vein thrombosis model in vivo. Circulation. 1997;96:1612-1615.
48. Schleef RR, Bevilacqua MP, Sawdey M, et al. Cytokine activation of vascular endothelium. Effects on tissue-type plasminogen activator and type 1 plasminogen activator inhibitor. J Biol Chem. 1988;263:5797-5803.
49. Sawdey MS, Loskutoff DJ. Regulation of murine type 1 plasminogen activator inhibitor gene expression in vivo. Tissue specificity and induction by lipopolysaccharide, tumor necrosis factor-alpha, and transforming growth factor-beta. J Clin Invest. 1991;88:1346-1353.
50. Yamamoto K, Loskutoff DJ. Fibrin deposition in tissues from endotoxin-treated mice correlates with decreases in the expression of urokinase-type but not tissue-type plasminogen activator. J Clin Invest. 1996;97:2440-2451.
51. ten Cate H. Pathophysiology of disseminated intravascular coagulation in sepsis. Crit Care Med. 2000;S9-S11.
52. Hermans PW, Hibberd ML, Booy R, et al. 4G/5G promoter polymorphism in the plasminogen-activator-inhibitor-1 gene and outcome of meningococcal disease. Meningococcal Research Group. Lancet. 1999;354:556-60.
53. Westendorp RG, Hottenga JJ, Slagboom PE. Variation in plasminogen-activator-inhibitor-1 gene and risk of meningococcal septic shock. Lancet. 1999;354:561-563.
54. Brandtzaeg P, Joo GB, Brusletto B, Kierulf P. Plasminogen activator inhibitor 1 and 2, alpha-2-antiplasmin, plasminogen, and endotoxin levels in systemic meningococcal disease. Thromb Res. 1990;57:271-278.
55. Mesters RM, Florke N, Ostermann H, Kienast J. Increase of plasminogen activator inhibitor levels predicts outcome of leukocytopenic patients with sepsis. Thromb Haemost. 1996;75:902-907.
56. Zimmerhackl LB, Rosales A, Hofer J, et al. Enterohemorrhagic Escherichia coli O26:H11-Associated Hemolytic Uremic Syndrome: Bacteriology and Clinical Presentation. Semin Thromb Hemost. 2010;36:586-593.
57. Karpman D, Sartz L, Johnson S. Pathophysiology of typical hemolytic uremic syndrome. Semin Thromb Hemost. 2010;36:575-585.
58. van Gorp E, Suharti C, ten Cate H, et al. Review: infectious diseases and coagulation disorders. J Infect Dis. 1999;180:176-186.
59. Aderem A, Ulevitch RJ. Toll-like receptors in the induction of the innate immune response. Nature. 2000;406:782-787.
60. Anas AA, Wiersinga WJ, de Vos AF, van der Poll T. Recent insights into the pathogenesis of bacterial sepsis. Neth J Med. 2010;68:147-152.
61. Vos FJ, Bleeker-Rovers CP, Sturm PD, et al. Endocarditis: effects of routine echocardiography during Gram-positive bacteraemia. Neth J Med. 2011;69:335-340.
62. Bhamarapravati N. Hemostatic defects in dengue hemorrhagic fever. Rev Infect Dis. 1989;11 Suppl 4:S826-S829.
63. Heller MV, Marta RF, Sturk A, et al. Early markers of blood coagulation and fbrinolysis activation in Argentine hemorrhagic fever. Thromb Haemost. 1995;73:368-373.
64. Mohanty D, Ghosh K, Nandwani SK, et al. Fibrinolysis, inhibitors of blood coagulation, and monocyte derived coagulant activity in acute malaria. Am J Hematol. 1997;54:23-29.
65. Chuttani K, Tischler MD, Pandian NG, et al. Diagnosis of cardiac tamponade after cardiac surgery: relative value of clinical, echocardi-ographic, and hemodynamic signs. Am Heart J. 1994;127:913-918.
66. Fera G, Semeraro N, De Mitrio V, Schiraldi O. Disseminated intravascular coagulation associated with disseminated cryptococcosis in a patient with acquired immunodefciency syndrome. Infection. 1993;21:171-173.
67. Schroder S, Spyridopoulos I, Konig J, et al. Thrombotic thrombocytopenic purpura (TTP) associated with a Borrelia burgdorferi infection. Am J Hematol. 1995;50:72-73.
68. Gardlund B. Randomised, controlled trial of low-dose heparin for prevention of fatal pulmonary embolism in patients with infectious diseases. The Heparin Prophylaxis Study Group.[see comments] Lancet. 1996;347:1357-1361.
69. Laing RB, Brettle RP, Leen CL. Venous thrombosis in HIV infection. [editorial] Int J STD AIDS. 1996;7:82-85.
70. Jenkins RE, Peters BS, Pinching AJ. Thromboembolic disease in AIDS is associated with cytomegalovirus disease.[letter] AIDS. 1991;5:1540-1542.
71. Drancourt M, George F, Brouqui P, Sampol J, Raoult D. Diagnosis of Mediterranean spotted fever by indirect immunofuorescence of Rickettsia conorii in circulating endothelial cells isolated with monoclonal antibody-coated immunomagnetic beads. J Infect Dis. 1992;166:660-663.
72. Keller TT, van Wissen M, Mairuhu AT, van Doornum GJ, Brandjes DP. Acute respiratory tract infections in elderly patients increase systemic levels of hemostatic proteins. J Thromb Haemost. 2007;5:1567-1569.
73. van Wissen M, Keller TT, Ronkes B, et al. Influenza infection and risk of acute pulmonary embolism. Thromb J. 2007;5:16.
74. Grau AJ, Urbanek C, Palm F. Common infections and the risk of stroke. Nat Rev Neurol. 2010;6:681-694.
75. Zoller B, Li X, Sundquist J, Sundquist K. Risk of pulmonary embolism in patients with autoimmune disorders: a nationwide follow-up study from Sweden. Lancet. 2011.
76. Hayes EB, Gubler DJ. Dengue and dengue hemorrhagic fever.[Review] Pediatr Infect Dis J. 1992;11:311-317.
77. Sumarmo, Wulur H, Jahja E et al. Clinical observations on virologically confirmed fatal dengue infections in Jakarta, Indonesia. Bull World Health Organ. 1983;61:693-701.
78. Kuberski T, Rosen L, Reed D, Mataika J. Clinical and laboratory observations on patients with primary and secondary dengue type 1 infections with hemorrhagic manifestations in Fiji. Am J Trop Med Hyg. 1977;26:775-783.
79. Limbos MA, Lieberman JM. Disseminated intravascular coagulation associated with rotavirus gastroenteritis: report of two cases.[see comments] Clin Infect Dis. 1996;22:834-836.
80. Anderson DR, Harrison L, Hirsh J. Evaluation of a portable prothrombin time monitor for home use by patients who require long-term oral anticoagulant therapy. Arch Intern Med. 1993;153:1441-1447.
81. McKay DG, Margaretten W. Disseminated intravascular coagulation in virus diseases. Arch Intern Med. 1967;120:129-152.
82. Linder M, Muller-Berghaus G, Lasch HG, Gagel C. Virus infection and blood coagulation. Thromb Diath Haemorrh. 1970;23:1-11.
83. Anderson DR, Schwartz J, Hunter NJ, et al. Varicella hepatitis: a fatal case in a previously healthy, immunocompetent adult. Report of a case, autopsy, and review of the literature. Arch Intern Med. 1994;154:2101-2106.
84. Clemens R, Pramoolsinsap C, Lorenz R, et al. Activation of the coagulation cascade in severe falciparum malaria through the intrinsic pathway. Br J Haematol. 1994;87:100-105.
85. Badesha PS, Saklayen MG. Hemolytic uremic syndrome as a presenting form of HIV infection. Nephron. 1996;72:472-475.
86. Ackerman AB, Chongchitnant N, Sanchez J, Guo Y. Infammatory diseases; Histologic diagnosis of infammatory skin diseases. Williams and Wilkins. 1997;170-186.
87. Lie JT. Vasculitis associated with infectious agents. Curr Opin Rheumatol. 1996;8:26-29.
88. Guillevin L, Lhote F, Gherardi R. The spectrum and treatment of virus-associated vasculitides. Curr Opin Rheumatol. 1997;9:31-36.
89. Golden MP, Hammer SM, Wanke CA, Albrecht MA. Cytomegalovirus vasculitis. Case reports and review of the literature. Medicine. 1994;73:246-255.
90. Ho DD, Rota TR, Andrews CA, Hirsch MS. Replication of human cytomegalovirus in endothelial cells. J Infect Dis. 1984;150:956-957.
91. Goodman MD, Porter DD. Cytomegalovirus vasculitis with fatal colonic hemorrhage. Arch Pathol Lab Med. 1973;96:281-284.
92. Foucar E, Mukai K, Foucar K, et al. Colon ulceration in lethal cytomegalovirus infection. Am J Clin Pathol. 1981;76:788-801.
93. Booss J, Dann PR, Winkler SR, et al. Mechanisms of injury to the central nervous system following experimental cytomegalovirus infection. Am J Otolaryngol. 1990;11:313-317.
94. Koeppen AH, Lansing LS, Peng SK, Smith RS. Central nervous system vasculitis in cytomegalovirus infection. J Neurol Sci. 1981;51:395-410.
95. Lin CS, Penha PD, Krishnan MN, Zak FG. Cytomegalic inclusion disease of the skin. Arch Dermatol. 1981;117:282-284.
96. Libman BS, Quismorio FPJ, Stimmler MM. Polyarteritis nodosa-like vasculitis in human immunodefciency virus infection. J Rheumatol. 1995;22:351-355.
97. Calabrese LH. Vasculitis and infection with the human immunodefciency virus. Rheum Dis Clin North Am. 1991;17:131-147.
98. Gherardi R, Belec L, Mhiri C, et al. The spectrum of vasculitis in human immunodefciency virus-infected patients. A clinicopathologic evaluation. Arthritis Rheum. 1993;36:1164-1174.
99. Sergent JS, Lockshin MD, Christian CL, et al. Vasculitis with hepatitis B antigenemia: long-term observation in nine patients. Medicine. 1976;55:1-18.
100. Carson CW, Conn DL, Czaja AJ, et al. Frequency and significance of antibodies to hepatitis C virus in polyarteritis nodosa. J Rheumatol. 1993;20:304-309.
101. Leruez-Ville M, Lauge A, Morinet F, et al. Polyarteritis nodosa and parvovirus B19. Lancet. 1994;344:263-264.
102. Nikkari S, Mertsola J, Korvenranta H, et al. Wegener's granulomatosis and parvovirus B19 infection. Arthritis Rheum. 1994;37:1707-1708.
103. Yoto Y, Kudoh T, Haseyama K, et al. Human parvovirus B19 infection in Kawasaki disease.[letter; comment] Lancet. 1994;344:58-59.
104. Levi MM, Eerenberg E, Lowenberg E, Kamphuisen PW. Bleeding in patients using new anticoagulants or antiplatelet agents: risk factors and management. Neth J Med. 2010;68:68-76.
105. Levi M, Levy M, Williams MD, et al. Prophylactic heparin in patients with severe sepsis treated with drotrecogin alfa (activated). Am J Respir Crit Care Med. 2007;176:483-490.
106. Abraham E, Reinhart K, Opal S, et al. Efficacy and safety of tifacogin (recombinant tissue factor pathway inhibitor) in severe sepsis: a randomized controlled trial. JAMA. 2003;290:238-247.