Involvement of coagulation and hemostasis in inflammatory bowel diseases

Current Vascular Pharmacology

Volumn 10, Issue 5, 2012, Pages 659-669

  Stadnicki, Antoni ^a,b  

^a MEDICAL UNIVERSITY OF SILESIA   (Poland)

^b District Hospital   (Poland)

Author keywords

Coagulation; Crohn's disease; Fibrinolysis; Heparin; Inflammatory bowel disease; Platelets; Risk factors; Thromboembolic complications

Indexed keywords

5,10 METHYLENETETRAHYDROFOLATE REDUCTASE (FADH2); BLOOD CLOTTING FACTOR 10; BLOOD CLOTTING FACTOR 10A; BLOOD CLOTTING FACTOR 11; BLOOD CLOTTING FACTOR 12A; BLOOD CLOTTING FACTOR 13; BLOOD CLOTTING FACTOR 13A; BLOOD CLOTTING FACTOR 5 LEIDEN; BLOOD CLOTTING FACTOR 5A; BLOOD CLOTTING FACTOR 7; BLOOD CLOTTING FACTOR 7A; BLOOD CLOTTING FACTOR 8A; BLOOD CLOTTING FACTOR 9; BLOOD CLOTTING FACTOR 9A; CORTICOSTEROID; ENOXAPARIN; HEPARIN; LOW MOLECULAR WEIGHT HEPARIN; PARNAPARIN; PLACEBO; PROTEINASE ACTIVATED RECEPTOR 1; PROTEINASE ACTIVATED RECEPTOR 2; PROTEINASE ACTIVATED RECEPTOR 3; PROTEINASE ACTIVATED RECEPTOR 4; PROTHROMBIN; THROMBIN; THROMBIN ACTIVATABLE FIBRINOLYSIS INHIBITOR; THROMBOPLASTIN; TISSUE FACTOR PATHWAY INHIBITOR; UNINDEXED DRUG;

ANTIINFLAMMATORY ACTIVITY; ARTICLE; BLEEDING; BLOOD CLOTTING; BLOOD CLOTTING DISORDER; CROHN DISEASE; ENDOTHELIAL DYSFUNCTION; ENTERITIS; FIBRIN CLOT; FIBRINOLYSIS; GENE MUTATION; HEMOSTASIS; HIGH RISK PATIENT; HUMAN; HYPERCOAGULABILITY; LABORATORY TEST; NONHUMAN; PATHOGENESIS; PREDICTIVE VALUE; PROTEIN DEGRADATION; RISK FACTOR; SYSTEMIC CIRCULATION; THROMBOCYTE ACTIVATION; THROMBOEMBOLISM; THROMBOPHILIA; ULCERATIVE COLITIS;

ANIMALS; ANTICOAGULANTS; BLOOD COAGULATION; COLITIS, ULCERATIVE; CROHN DISEASE; DOSE-RESPONSE RELATIONSHIP, DRUG; FACTOR XIII; HEMOSTASIS; HEPARIN; HUMANS; PREDICTIVE VALUE OF TESTS; RISK FACTORS; THROMBOEMBOLISM;

EID: 84864558645     PISSN: 15701611     EISSN: 18756212     Source Type: Journal    
DOI: 10.2174/157016112801784495     Document Type: Article

References (122)

1. Sartor RB. Mechanism of disease: pathogenesis of Crohn's disease and ulcerative colitis. Nature Clin Pract Gastroenterol Hepatol 2006; 3: 390-407.
2. Baumgart DC, Carding SR. Gastroenterology 1. Inflammatory bowel disease: cause and immunobiology. Lancet 2007; 369: 1627-40.
3. Danese S, Papa A, Saibeni S, Repici A, Malesci A, Vecchi M. Inflammation and coagulation in inflammatory bowel disease: the clot thickens. Am J Gastroenterol 2007; 102: 174-86.
4. Hoffman M, Monroe DM. Coagulation: a modern view of hemostasis. Hematol Oncol Clin North Am 2007; 21: 1-11.
5. Colman RW. Are hemostasis and thrombosis two sides of the same coin? JEM 2006; 203: 493-5.
6. Oliver JA, Monroe DM, Roberts HR, Hoffman M. Thrombin activates factor XI on activated platelets in the absence of factor XII. Arterioscler Thromb Vasc Biol 1999; 19: 170-7.
7. Bouma BN, Mosnier LO. Thrombin activatable fibrinolysis inhibitor (TAFI) at the interface between coagulation and fibrinolysis. Pathophysiol Haemost Thromb 2004; 33: 375-81.
8. Lee JC, Spittell JA, Sauer WG, Owen CA, Thompson JH. Hypercoagulability associated with chronic ulcerative colitis: changes in blood coagulation factors. Gastroenterology 1968; 54: 76-85.
9. Lam A, Borda IT, Inwood MJ, Thomson S. Coagulation studies in ulcerative colitis and Chron's disease. Gastroenterology 1975; 68: 245-51.
10. Knot EA, ten Cate JW, Bruin T, Iburg AH, Tytgat GN. Antithrombin III metabolism in two colitis patients wit acquired antithrombin III deficiency. Gastroenterology 1985; 89: 421-5.
11. Edwards RL, Levine JB, Green R, et al. Activation of blood coagulation in Crohn's disease. Increased plasma fibrinopeptide A levels and enhanced generation of monocyte tissue factor activity. Gastroenterology 1987; 92: 329-37.
12. Hudson M, Hutton RA, Wakefield AJ, Sawyerr AM, Pounder RE. Evidence for activation of coagulation in Crohn's disease. Blood Coagul Fibrinolysis 1992; 3:773-8.
13. Souto JC, Martinez E, Roca M, et al. Prothrombotic state and signs of endothelial lesion in plasma of patients with inflammatory bowel disease. Dig Dis Sci 1995; 40:1883-9.
14. van Bodegraven AA, Tuynman HA, Schoorl M, Kruishoop AM, Bartels PC. Fibrinolytic split product, fibrinolysis and factor XIII activity in inflammatory bowel disease. Scand J Gastroenterol 1995; 30: 580-5.
15. Chamouard P, Grunebaum L, Wiesel ML, et al. Prothrombin fragment 1+2 and thrombin-antithrombin III complex as markers of activation of blood coagulation in inflammatory bowel diseases. Eur J Gastroenterol Hepatol 1995; 7: 1183-8.
16. Chiarantini F, Valanzano R, Liotta AA, et al. Hemostatc abnormalities in inflammatory bowel disease. Thromb Res 1996; 82: 137-46.
17. van Bodegraven AA, Schoorl M, Linskens RK, Bartels PC, Tuynman HA. Persistent activation of coagulation and fibrinolysis after treatment of active ulcerative colitis. Eur J Gastroenterol Hepatol 2002; 14: 413-8.
18. Knot EA, ten Cate JW, Leeksma OC, Tytgat GN, Vreeken J. No evidence for the prethrombotic state in stable inflammatory bowel disease. J Clin Pathol 1983; 36: 1387-90.
19. Novacek G, Kapiotis S, Moser G, Speiser W, Gangl A, Vogelsang H. No evidence of activated blood coagulation in Crohn's disease. Eur J Gastroenterol Hepatol 1997:9: 963-7.
20. Stadnicki A, Gonciarz M, Niewiarowski TJ, et al. Activation of plasma contact and coagulation systems and neutrophils in the active phase of ulcerative colitis. Dig Dis Sci 1997; 42: 2356-66.
21. Saibeni S, Saladino V, Cantarangkul V et al. Increased thrombin generation in inflammatory bowel diseases. Thromb Res 2001; 125: 278-82.
22. Larsen TB, Nielsen JN, Fredholm L, et al. Platelets and anticoagulant capacity in patients with inflammatory bowel disease. Pathophysiol Haemost Thromb 2002; 32: 92-6.
23. Aadland E, Odegaard OR, Roseth A, Try K. Free protein S deficiency in patients with Cronh's disease. Scand J Gastroenterol 1994; 29: 333-5.
24. Saibeni S, Vecchi M, Valsecchi C, et al. Reduced free protein S levels in patients with inflammatory bowel disease. Prelevalece, clinical relevance, and role of anti-protein S antibodies. Dig Dis Sci 2001; 46: 637-43.
25. Mazlam MZ, Hodgson HJ. Interaction between interleukin-6, interleukin-1 beta, plasma C-reactive protein values, and in vitro Creactive protein generation in patients with inflammatory bowel disease. Gut 1994; 35: 77-86.
26. Wakefield A, Sawyerr A, Dhillon A, et al. Pathogenesis of Crohn's disease: multifocal gastrointestinal infarction. Lancet 1989; 2:1057-62.
27. Wakefield A, Sabkey EA, Dhillon A, et al. Granulomatous vasculitis in Crohn's disease. Gastroenterology 1991; 100: 1279-87.
28. More L, Sim R, Hudson M, et al. Immunohistochemical study of tissue factor expression in normal intestine and idiopathic inflammatory bowel disease. J Clin Pathol 1993; 46: 703-8.
29. Dhillon AP, Anthony A, Sim R, et al. Mucosal capillary thrombi in rectal biopsies. Histopathology 1992: 21: 127-33.
30. Ichinose A. Physiopathology and regulation of factor XIII. Thromb Haemost 2001; 86: 57-65.
31. Hudson M, Wakefield AJ, Hutton RA, et al. Factor XIIIA subunit and Crohn's disease. Gut 1993; 34: 75-9.
32. Stadnicki A, Kloczko J, Nowak A, Sierka E, Sliwinski Z. Factor XIII subunits in relation to some other hemostatic parameters in ulcerative colitis. Am J Gastroenterol 1991; 86: 690-3.
33. Hayat M, Ariëns RA, Moayyedi P, Grant PJ, O' Mahony S. Coagulation factor XIII and markers of thrombin generation and fibrinolysis in patients with inflammatory bowel disease. Eur J Gastroenterol Hepatol 2002; 14: 249-56.
34. Stadnicki A, Kłoczko J, Nowak A, Sierka E. Alterations of haemostatic parameters in special references to factor XIII and fibronectin in patients with ulcerative colitis. Eur J Gastroenterol Hepatol 1992; 4: 743-6.
35. D'Argenio G, Biancone L, Cosenza V, et al. Transglutaminases in Cronh's disease. Gut 1995; 37: 690-5.
36. Sheppach W, Sommer H, Kirchner T, et al. Effect of butyrate enemas on the colonic mucosa in distal ulcerative colitis. Gastroenterology 1992; 103: 51-6.
37. Brickbichler PJ, Orr JR, Patterson MK, Conoway E, Carter HA, Maxwell MD. Enhanced transglutaminase activity is transformed human lung fibroblast cells after exposure to sodium butyrate. Biochim Biophys Acta 1983; 763: 27-34.
38. D' Argenio G, Gosenza V, Sorrentini I, et al. Butyrate, mesalamine and factor XIII in experimental colitis in the rats: effect on transglutaminase activity. Gastroenterology 1994; 106: 399-404.
39. Suzuki R, Toda K, Takamura Y. Dynamic of blond coagulation factor XIII in ulcerative colitis and preliminary study of factor XIII concentrate Blut 1989; 59: 162-4.
40. Devani M, Cugno M, Vecchi M, et al. Kallikrein-kinin system activation in Crohn's disease: Differences in intestinal and systemic markers. Am J Gastroenterol 2002; 97: 2026-32.
41. Kyriakou DS, Aleksandrakis MG, Passam FH, et al. Acquired inhibitors of coagulation factors in patients with gastrointestinal diseases. Eur J Gastroenterol Hepatol 2002; 14: 1383-7.
42. Kume K, Yamasaki M, Tashiro M, Yoshikawa I, Otsuki M. Activation of coagulation and fibrinolysis secondary to bowel inflammation in patients with ulcerative colitis. Internal Medicine 2007; 46: 1323-9.
43. Stadnicki A. Pastucha E, Nowaczyk G, et al. Immunolocalization and expression of kinin B1 and B2 receptors in human inflammatory bowel disease. Am J Physiol 2005; 289: G361-6.
44. Gardiner KR, Halliday MI, Barclay GR, et al. Significance of systemic endotoxemia in inflammatory bowel disease. Gut 1995; 36: 897-901.
45. Andoh A, Tsujikawa T, Hata K, et al. Elevated circulating platelet-derived microplates in patients with active inflammatory bowel disease. Am J Gastroenterol 2005; 100: 2042-8.
46. Stadnicki A, Khan M, Plewka D, et al. Tissue factor expression during peptidoglycan-induced enterocolitis in Lewis rats. Gut 2003; 52 (SupplVI): Abs. G 068.
47. Yoshida H, Russell J, Granger DN. Thrombin mediates the extraintestinal thrombosis associated with experimental colitis. Am J Physiol 2008; 265: G904-8.
48. Yoshida H, Granger DN. Inflammatory bowel diseases: a paradigm for the link between coagulation and inflammation. Inflamm Bowel Dis 2009; 15: 1245-55.
49. Anthoni C, Russell J, Wood KC, et al. Tissue factor: a mediator of inflammatory cell recruitment, tissue injury, and thrombus formation in experimental colitis. J Exp Med 2007; 204: 1595-601.
50. Sharma L, Melis E, Hickey MJ, et al. The cytoplasmic domain of tissue factor contributes to leukocyte recruitment and death in endotoxemia. Am J Pathol 2004; 165: 331-40.
51. Steinhoff M, Buddenkotte J, Shpacovitch V, et al. Proteinase activated receptors: transducers of proteinase mediated signaling in inflammation and immune response. Endoc Rev 2005; 26: 1-43.
52. Borensztajn K, Peppelenbosch MP, Spek CA. Coagulation and factor Xa signaling: the link between coagulation and inflammatory bowel disease? Trends Pharmacol Sci 2009; 30: 8-16.
53. Faioni FM, Ferrero S, Fontana G, et al. Expression of endothelial protein C receptor and thromomodulin in the intestinal tissue of patients with inflammatory bowel disease. Crit Care Med 2004; 32 (Suppl 5): S266-70.
54. Yoshida H, Russell J, Stokes KY, et al. Role of the protein C pathway in the extraintestinal thrombosis associated with murine colitis. Gastroenterology 2008; 135: 882-8.
55. Biloduane LM, Hamm HE. Regulation of protease-activated receptor PAR1 and PAR4 signaling in human platelets by compartmentalized cyclic nucleotide action. J Pharm Exp Ther 2007; 322: 778-88.
56. de Jong E, Porte RJ, Knot EA, Verheijen JH, Dees J. Disturbed fibrinolysis in patients with inflammatory bowel disease. A study of blood plasma, colon mucosa, and faeces. Gut 1989; 30: 188-94.
57. Gris JC, Schved JF, Raffanel C, Dubois A, Ribard D, Balmes JL. Impaired fibrinolytic response to the venous occlusion test in patients with cryptogenic colitis. Gastroenterol Clin Biol 1991; 15: 933-8.
58. Koutroubakis IE, Sfiridaki A, Tsiolakidou G, Coucoutsi C, Theodoropoulou A, Kouroumalis EA. Plasma thrombin-activatable fibrinolysis inhibitor and plasminogen activator inhibitor-1 levels in inflammatory bowel disease. Eur J Gastroenterol Hepatol 2008; 20: 912-6.
59. Saibeni S, Bottasso B, Spina L, et al. Assessment of thrombinactivatable fibrilolysis inhibitor (TAFI) plasma levels in inflammatory bowel diseases. Am J Gastroenterol 2004; 99: 1966-70.
60. Saibeni S, Ciscato C, Vecchi M, et al. Antibodies to tissue-type plasminogen activator (t-PA) in patients with inflammatory bowel disease: high prevalence, interaction with functional domains of t-PA and possible implications in thrombosis. J Thromb Haemost 2006; 4: 1510-6.
61. Stadnicki A, Kacperek T, Nowak A, et al. Modulatory effect of the gut on fibrinolysis and fibrinogen derivatives. Scand. J Gastroenterol 22; 1987: 539-42.
62. Rahr HB, Sorensen JV, Larsen JF, Jensen FS, Bredahl C. Plasminogen activators and plasminogen activator inhibitor in portal blood from patients with and without gastric malignancy. Scand J Gastroenterol 1994; 29: 516-21.
63. de Bruin PA, Crama-Bohbout G, Verspaget HW, et al. Plasminogen activators in the intestine of patients with inflammatory bowel disease. Thromb Haemost 1988; 60: 262 6.
64. Colman RW. Contact activation (kallikrein-kinin) pathway: multiple physiologic and pathophysiologic activities. In: Colman RW, Marder VJ, Cloves AW, George JN, Ed. Hemostasis and Thrombosis. Basic Principles and Clinical Practice. 5th ed. Philadelphia: Lippincott Wiliams &Wilkins 2006; pp. 103-21.
65. Meucci G, Pareti F, Vecchi M, et al. Serum von Willebrant factor levels in patients with inflammatory bowel disease are related to systemic inflammation. Scand J Gastroenterol 1999: 34: 287-90.
66. Boehme MW, Autschbach F, Zuna I, et al. Elevated serum levels and reduced immunohistochemical expression of thrombomodulin in active ulcerative colitis. Gastroenterology 1997; 113: 107-17.
67. Wan der Wouwer D, Collen D, Conway EM. Thrombomodulinprotein C-EPCR system: integrated to regulate coagulation and inflammation. Arterioscler Thromb Vasc Biol 2004; 24: 1374-83.
68. Harries AD, Beeching NJ, Rogerson Sr, et al. The platelet count as a simple measure to distinguish inflammatory bowel disease from infective diarrhea. J Infect 1991; 22: 247-50.
69. Heits F, Stahl M, Ludwig D, et al. Elevated serum thrombopoetyn and interleukin-6 concentration in thrombocytosis associated with inflammatory bowel disease. Cytokine Res 1999; 19: 757-60.
70. Webberley MJ, Hart MT, Melikian V, et al. Thromboembolism in inflammatory bowel disease: role of platelets. Gut 1993; 34: 247-51.
71. Collins CE, Rampton DS, Rogers J, et al. Platelet aggregation and neutrophil sequestration in the mesenteric circulation in inflammatory bowel disease. Eur J Gastroenterol Hepatol 1997; 9: 1213-17.
72. Zahavi J, Kakkar VV.-thromboglobulin-a specific marker of in vivo platelet release reaction. Thromb Haemost 1980; 44: 23-9.
73. Collins CE, Cahill MR, Newland AC, Rampton DS. Platelets circulate in an activated state in inflammatory bowel disease. Gastroenterology 1994; 106: 840-5.
74. Danese S, Katz JA, Saibeni S, et al. Activated platelets are the source of elevated levels of soluble CD40 ligand in the circulation of inflammatory bowel disease patients. Gut 2003; 52: 1435-41.
75. Danese S, de La Motte C, Sturm A, et al. Platelets trigger a CD40-dependent inflammatory response in the microvasculature of inflammatory bowel disease patients. Gastroenterology 2003; 124: 1249-64.
76. Fagerstam JP, Whiss PA, Strom M, Andersson RG. Expression of platelet P-selectin and detection of soluble P-selectin, NPY and RANTES in patients with inflammatory bowel disease. Inflamm Res 2000; 49: 466-72.
77. Irving PM, Macey MG, Shah U, et al. Formation of platelet-leukocyte aggregates in inflammatory bowel disease. Inflamm Bowel Dis 2004; 10: 361-72.
78. Talbot RW, Heppell J, Dozois RR, Beart RW. Vascular complications of inflammatory bowel disease. Mayo Clin Proc 1986; 61: 140-5.
79. Jackson LM, O'Gorman PJ, O'Connell J, Cronin CC, Cotter KP, Shanahan F. Thrombosis in inflammatory bowel disease: clinical setting, procoagulant profile and factor V Leiden. QJM 1997; 90: 183-8.
80. Stadnicki A, Bojko B, Myczkowska K, Witaliska-abuzek J. Some risk factors of thrombotic complication in patients with ulcerative colitis. Wiad Lek 2003; 8: 341-7.
81. Bargen JA, Barker NW. Extensive arterial and venous thrombosis complicating chronic ulcerative colitis. Arch Intern Med 1936; 58: 17-31.
82. Bernstein CN, Blanchard JF, Houston DS, Wajda A. The incidence of deep venous thrombosis and pulmonary embolism among patients with inflammatory bowel disease: a population-based cohort study. Thromb Haemost 2001; 85: 430-4.
83. Miehsler W, Reinisch W, Valic E, et al. Is inflammatory bowel disease an independent and disease specific risk factor for thromboembolism? Gut 2004; 53: 542-8.
84. Nguyen GC, Sam J. Rising prevalence of venous thromboembolism and its impact on mortality among hospitalized inflammatory bowel disease patients. Am J Gastroenterl 2008; 103: 2272-80.
85. Grainge MJ, West J, Card TR. Venous thromboembolism during active disease and remission in inflammatory bowel disease: a cohort study. Lancet 2010; 375: 657-63.
86. Novacek G, Weltermann A, Sobala A et al. Inflammatory bowel disease is a risk factor for recurrent venous thromboembolism. Gastroenterology 2010; 139: 779-87.
87. Quera R, Shanahan F, Thromboembolism-an important manifestation of inflammatory bowel disease. Am J Gastroenterol 2004; 99: 1971-3.
88. Vrij AA, Rijken J, van Wersch JW, Stockbrügger RW. Coagulation and fibrinolysis in inflammatory bowel disease and in giant cell arteritis. Pathophysiol Haemost Thromb 2003; 33: 75-83.
89. Bernstein CN, Wajda A, Blanchard JF. The incidence of arterial thromboembolic disease in inflammatory bowel disease: a population based study. Clin Gastroenterol Hepatol 2008; 6: 41-5.
90. Kappelman MD, Horvath-Puho E, Sandler RS et al. Thromboembolic risk among Danish children and adults with inflammatory bowel disease: a population-based nationwide study. Gut 2011; 60: 937-43.
91. Solem CA, Loftus EV, Tremaine WJ, Sandborn WJ. Venous thromboembolism in inflammatory bowel disease. Am J Gastroenterol 2004; 99: 97-101.
92. Bjerregaard LT, Nederby NJ, Fredholm L, Brandslund I, Munkholm P, Hey H. Hyperhomocysteinaemia, coagulation pathway activation and thrombophilia in patients with inflammatory bowel disease. Scand J Gastroenterol 2002; 37: 62-7.
93. van Bodegraven AA, Meuwissen SG. Lipoprotein (a), thrombophilia and inflammatory bowel disease. Eur J Gastroenterol Hepatol 2001; 13: 1407-9.
94. Aichbichler BN, Petritsch W, Reicht GA et al. Anticardiolipin antibodies in patients with inflammatory bowel disease. Dig Dis Sci 1999; 44: 852-6.
95. Papa A, De StefanoV, Gasbarrini A, Gasbarrini. Factor V Leiden is no more frequent in inflammatory bowel disease. Eur J Gastroeterol Hepatol 2000; 12: 821-2.
96. Koutroubakis IE, Sfiridaki A, Mouzas IA, et al. Resistance to activated protein C and low levels of free protein S in Greak patients with inflammatory bowel disease. Am J Gastroenterol 2000; 95: 190-4.
97. Liebman HA, Kashani M, Sutherland D, MeGehee W, Kam AL. The factor V Leiden mutation increases the risk of venous thrombosis in patients with inflammatory bowel disease. Gastroenterology 1998; 115: 830-4.
98. Papa A, De Stefano V, Gasbarrini A, et al. Prelevalence of factor V Leiden and the G20210A prothrombin-gene mutation in inflammatory bowel disease Blood Coagul Fibrinolysis 2000; 11: 499-503.
99. Guedon C, Le Camp Duhes V, Lalaude O, Menard JF, Lerebous E, Borg JY. Prothrombotic inherited abnormalities other than factor V Leiden mutation do not play a role in venous thrombosis in inflammatory bowel disease. Am J Gastroenterol 2001; 96: 1448-54.
100. Thompson NP, Wakefield AJ, Pounder RE. Inherited disorders of coagulation appear to protect against inflammatory bowel disease. Gastroenterology 1995; 108: 1011-15.
101. Helio T, Vartivaarara U, Halme IA, et al. Arg506Gln factor V mutation and Val134Leu factor XIII polymorphism in Finish patients with inflammatory bowel disease. Scand J Gastroenterol 1999; 94: 685-90.
102. Carty E, MacEy M, Rampton DS. Inhibition of platelet activation by 5-aminosalicylic acid in inflammatory bowel disease. Aliment Pharmacol Ther 2000; 14: 1169-79.
103. Winther K, Bondesen S, Hansen SH et al. Lack effect of 5-aminosalicylic acid on platelet aggregation and fibrinolytic activity in vivo and in vitro. Eur J Clin Pharmacol 1987; 33: 419-22.
104. Maxwell SR, Moots LJ, Kendall MJ. Corticosteroids: do they damage the cardiovascular system? Postgrad Med J 1994; 70:863-70.
105. Bombeli T, Muller M, Straub PW, et al. Cyclosporine-induced detachment of vascular endothelial cells initiates the intrinsic coagulation system in plasma and whole blood. J Lab Clin Med 1996; 127: 621-34.
106. Hommes DW, van Dullemen HM, Levi M, et al. Beneficial effect of treatment with a monoclonal anti-tumor necrosis factor-{replacement character}{replacement character} antibody on markers of coagulation and fibrinolysis in patients with Cronh's disease. Haemostasis 1997; 27: 269-77.
107. Danese S, Sans M, Scaldaferri F, et al. TNF-{replacement character}{replacement character} blockade down-regulates the CD40/CD40L pathway in the mucosal microcirculation: a novel anti-inflammatory mechanism of infliximab in Crohn's disease. J Immunol 2006; 176: 2617-24.
108. Zavgorogniy L, Mustgat A. Application of anticoagulant in the complex treatment of ulcerative colitis. Klein Med 1982; 60: 74-80.
109. Gaffyney PR, Doyle CT, Gaffyney A, et al. Paradoxical response to heparin in 10 patients with ulcerative colitis. Am J Gastroenterol 1995; 90: 220-3.
110. Korzenik JR. Heparin: an emerging counterintuitive therapy for inflammatory bowel disease. Curr Treat Options Gastroenterol 2000; 3: 95-8.
111. Panes J, Esteve M, Cabre E, et al. Comparison of heparin and steroid in the treatment of moderate and severe ulcerative colitis. Gastroenterology 2000; 119: 903-8.
112. Dotan I, Hallak A, Arber N, et al. Low-dose low molecular weight heparin (enoxaparin) is effective as adjuvant treatment in active ulcerative colitis: an open trial. Dig Dis Sci 2001; 46: 2239-44.
113. Bloom S, Kiilerich S, Lasse MR, et al. Low molecular weight heparin (tinzaparin) vs. placebo in the treatment of mild to moderately active ulcerative colitis. Aliment Pharmacol Ther 2004; 19: 871-8.
114. Pastorelli L, Saibeni S, Spina L, et al. Oral-colonic release low-molecular weight heparin: an initial open study of Parnaparin MMX for the treatment of mild-to moderate left-sided ulcerative colitis. Aliment Pharmacol Ther 2008; 28: 581-88.
115. Tytgat GN, Van Nueten L, Ven de Velde I, et al. Efficacy and safety of oral ridogrel in the treatment of ulcerative colitis: two multicenter randomized, double blind studies. Aliment Pharmacol Ther 2002; 16: 87-99.
116. Kondo M, Hotta T, Takemura S, Yoshikawa T, Fukumuro K. Treatment of ulcerative colitis by the direct administration of antifibrinolytic agent as an enema. Hepatogastroenterology 1981; 28: 270-3.
117. Stadnicki A. A role of fibrinolysis in pathogenesis of gut diseases. Pol Arch Med Wewn 1987; 87: 347-54.
118. Lorenz R, Heinmullr M, Classen M, Tornieporth N, Gain T. Substitution of factor XIII: a therapeutic approach to ulcerative colitis. Haemostasis 1991; 21: 5-9.
119. Oshitani N, Nakamura S, Matsumoto T, Kobyashi K, Kitano A. Treatment of Crohn's disease fistulas with coagulation factor XIII. Lancet 1996; 347: 119-20.
120. Bregenzer N, Caesar I, Andus T, et al. Lack of clinical efficacy of additional factor XIII treatment in patients with steroid refractory colitis. Z Gastroenterol 1999; 37: 999-1004.
121. Zitomersky NL, Verhave M, Trenor CC. Thrombosis and inflammatory bowel disease: a call for improved awareness and prevention. Inflamm Bowel Dis 2011; 17:458-70.
122. Geerts WH, Bergqvist D, Pineo GF, et al. Prevention of venous thromboembolism: American College of Chest Physicians. Evidence-Based Clinical Practice Guidelines, 8 ed. Chest 2008; 133: 381S-451S.