Venous thromboembolism in cirrhosis

Clinical and Applied Thrombosis/Hemostasis

Volumn 20, Issue 2, 2014, Pages 169-178

  Yang, Zhineng J ^a   Costa, Karen A ^a   Novelli, Enrico M ^b,c   Smith, Roy E ^c  

^a PRESBYTERIAN UNIVERSITY HOSPITAL   (United States)

^b Hemophilia Center of Western PA   (United States)

^c UNIVERSITY OF PITTSBURGH MEDICAL CENTER   (United States)

Author keywords

anticoagulation; cirrhosis; coagulopathy; venous thromboembolism

Indexed keywords

ANTIVITAMIN K; ENOXAPARIN; LOW MOLECULAR WEIGHT HEPARIN; NADROPARIN;

ANTICOAGULATION; ARTICLE; BLEEDING; COMORBIDITY; DEMOGRAPHY; DISEASE PREDISPOSITION; FIBRINOLYSIS; INCIDENCE; LIVER CIRRHOSIS; PRIORITY JOURNAL; PROPHYLAXIS; RISK FACTOR; VENOUS THROMBOEMBOLISM;

ANTICOAGULATION; CIRRHOSIS; COAGULOPATHY; VENOUS THROMBOEMBOLISM;

COMORBIDITY; HUMANS; INCIDENCE; LIVER CIRRHOSIS; RISK FACTORS; VENOUS THROMBOEMBOLISM;

EID: 84893487941     PISSN: 10760296     EISSN: 19382723     Source Type: Journal    
DOI: 10.1177/1076029612461846     Document Type: Article

References (77)

1. Kim WR, Brown RS, Terrault NA, El-Serag H. Burden of liver disease in the United States: summary of a workshop. Hepatology. 2002 ; 36 (1). 227-242
2. Tripodi A, Mannucci PM. The coagulopathy of chronic liver disease. N Engl J Med. 2011 ; 365 (2). 147-156
3. Roberts LN, Patel RK, Arya R. Haemostasis and thrombosis in liver disease. Br J Haematol. 2010 ; 148 (4). 507-521
4. Northup PG, McMahon MM, Ruhl AP, et al. Coagulopathy does not fully protect hospitalized cirrhosis patients from peripheral venous thromboembolism. Am J Gastroenterol. 2006 ; 101 (7). 1524-1528
5. Gulley D, Teal E, Suvannasankha A, Chalasani N, Liangpunsakul S. Deep vein thrombosis and pulmonary embolism in cirrhosis patients. Dig Dis Sci. 2008 ; 53 (11). 3012-3017
6. Garcia-Fuster MJ, Abdilla N, Fabia MJ, Fernández C, Oliver V, Forner MJ. Venous thromboembolism and liver cirrhosis [In Spanish]. Rev Esp Enferm Dig. 2008 ; 100 (5). 259-262
7. Wu H, Nguyen GC. Liver cirrhosis is associated with venous thromboembolism among hospitalized patients in a nationwide US study. Clin Gastroenterol Hepatol. 2010 ; 8 (9). 800-805
8. Dabbagh O, Oza A, Prakash S, Sunna R, Saettele TM. Coagulopathy does not protect against venous thromboembolism in hospitalized patients with chronic liver disease. Chest. 2010 ; 137 (5). 1145-1149
9. Sogaard KK, Horvath-Puho E, Gronbaek H, Jepsen P, Vilstrup H, Sørensen HT. Risk of venous thromboembolism in patients with liver disease: a nationwide population-based case-control study. Am J Gastroenterol. 2009 ; 104 (1). 96-101
10. Kearon C. Natural history of venous thromboembolism. Circulation. 2003 ; 107 (23 suppl 1). I22 - I30
11. Castelino DJ, Salem HH. Natural anticoagulants and the liver. J Gastroenterol Hepatol. 1997 ; 12 (1). 77-83
12. Deitcher SR. Interpretation of the international normalised ratio in patients with liver disease. Lancet. 2002 ; 359 (9300). 47-48
13. Robert A, Chazouilleres O. Prothrombin time in liver failure: time, ratio, activity percentage, or international normalized ratio?. Hepatology. 1996 ; 24 (6). 1392-1394
14. Tripodi A, Baglin T, Robert A, et al. Reporting prothrombin time results as international normalized ratios for patients with chronic liver disease. J Thromb Haemost. 2010 ; 8 (6). 1410-1412
15. Trotter JF, Brimhall B, Arjal R, Phillips C. Specific laboratory methodologies achieve higher model for endstage liver disease (MELD) scores for patients listed for liver transplantation. Liver Transpl. 2004 ; 10 (8). 995-1000
16. Glassock RJ. Prophylactic anticoagulation in nephrotic syndrome: a clinical conundrum. J Am Soc Nephrol. 2007 ; 18 (8). 2221-2225
17. Caldwell SH, Hoffman M, Lisman T, et al. Coagulation disorders and hemostasis in liver disease: pathophysiology and critical assessment of current management. Hepatology. 2006 ; 44 (4). 1039-1046
18. Peck-Radosavljevic M, Wichlas M, Zacherl J, et al. Thrombopoietin induces rapid resolution of thrombocytopenia after orthotopic liver transplantation through increased platelet production. Blood. 2000 ; 95 (3). 795-801
19. Tonda R, Galan AM, Pino M, et al. Hemostatic effect of activated recombinant factor VII (rFVIIa) in liver disease: studies in an in vitro model. J Hepatol. 2003 ; 39 (6). 954-959
20. Escolar G, Cases A, Vinas M, et al. Evaluation of acquired platelet dysfunctions in uremic and cirrhotic patients using the platelet function analyzer (PFA-100): influence of hematocrit elevation. Haematologica. 1999 ; 84 (7). 614-619
21. Ferro D, Quintarelli C, Lattuada A, et al. High plasma levels of von Willebrand factor as a marker of endothelial perturbation in cirrhosis: relationship to endotoxemia. Hepatology. 1996 ; 23 (6). 1377-1383
22. Lisman T, Bongers TN, Adelmeijer J, et al. Elevated levels of von Willebrand factor in cirrhosis support platelet adhesion despite reduced functional capacity. Hepatology. 2006 ; 44 (1). 53-61
23. Dong JF. Cleavage of ultra-large von Willebrand factor by ADAMTS-13 under flow conditions. J Thromb Haemost. 2005 ; 3 (8). 1710-1716
24. Mannucci PM, Canciani MT, Forza I, Lussana F, Lattuada A, Rossi E. Changes in health and disease of the metalloprotease that cleaves von Willebrand factor. Blood. 2001 ; 98 (9). 2730-2735
25. Tripodi A, Salerno F, Chantarangkul V, et al. Evidence of normal thrombin generation in cirrhosis despite abnormal conventional coagulation tests. Hepatology. 2005 ; 41 (3). 553-558
26. Lisman T, Bakhtiari K, Pereboom IT, Hendriks HG, Meijers JC, Porte RJ. Normal to increased thrombin generation in patients undergoing liver transplantation despite prolonged conventional coagulation tests. J Hepatol. 2010 ; 52 (3). 355-361
27. Gatt A, Riddell A, Calvaruso V, Tuddenham EG, Makris M, Burroughs AK. Enhanced thrombin generation in patients with cirrhosis-induced coagulopathy. J Thromb Haemost. 2010 ; 8 (9). 1994-2000
28. Tripodi A, Primignani M, Chantarangkul V, et al. Thrombin generation in patients with cirrhosis: the role of platelets. Hepatology. 2006 ; 44 (2). 440-445
29. Tripodi A, Legnani C, Chantarangkul V, Cosmi B, Palareti G, Mannucci PM. High thrombin generation measured in the presence of thrombomodulin is associated with an increased risk of recurrent venous thromboembolism. J Thromb Haemost. 2008 ; 6 (8). 1327-1333
30. Tripodi A, Legnani C, Palareti G, Chantarangkul V, Mannucci PM. More on: high thrombin generation and the risk of recurrent venous thromboembolism. J Thromb Haemost. 2009 ; 7 (5). 906-907
31. Tripodi A, Primignani M, Chantarangkul V, et al. An imbalance of pro- vs anti-coagulation factors in plasma from patients with cirrhosis. Gastroenterology. 2009 ; 137 (6). 2105-2111
32. Dittman WA, Majerus PW. Structure and function of thrombomodulin: a natural anticoagulant. Blood. 1990 ; 75 (2). 329-336
33. Levin EG, Santell L, Osborn KG. The expression of endothelial tissue plasminogen activator in vivo: a function defined by vessel size and anatomic location. J Cell Sci. 1997 ; 110 (pt 2). 139-148
34. Binder BR, Christ G, Gruber F, et al. Plasminogen activator inhibitor 1: physiological and pathophysiological roles. News Physiol Sci. 2002 ; 17: 56-61
35. Chandler WL, Alessi MC, Aillaud MF, Henderson P, Vague P, Juhan-Vague I. Clearance of tissue plasminogen activator (TPA) and TPA/plasminogen activator inhibitor type 1 (PAI-1) complex: relationship to elevated TPA antigen in patients with high PAI-1 activity levels. Circulation. 1997 ; 96 (3). 761-768
36. Leebeek FW, Kluft C, Knot EA, de Maat MP, Wilson JH. A shift in balance between profibrinolytic and antifibrinolytic factors causes enhanced fibrinolysis in cirrhosis. Gastroenterology. 1991 ; 101 (5). 1382-1390
37. vanDeWater L, Carr JM, Aronson D, McDonagh J. Analysis of elevated fibrin(ogen) degradation product levels in patients with liver disease. Blood. 1986 ; 67 (5). 1468-1473
38. Hu KQ, Yu AS, Tiyyagura L, Redeker AG, Reynolds TB. Hyperfibrinolytic activity in hospitalized cirrhotic patients in a referral liver unit. Am J Gastroenterol. 2001 ; 96 (5). 1581-1586
39. Lisman T, Leebeek FW, Mosnier LO, et al. Thrombin-activatable fibrinolysis inhibitor deficiency in cirrhosis is not associated with increased plasma fibrinolysis. Gastroenterology. 2001 ; 121 (1). 131-139
40. Colucci M, Binetti BM, Branca MG, et al. Deficiency of thrombin activatable fibrinolysis inhibitor in cirrhosis is associated with increased plasma fibrinolysis. Hepatology. 2003 ; 38 (1). 230-237
41. Kahn SR, Lim W, Dunn AS, et al. Prevention of VTE in nonsurgical patients: antithrombotic therapy and prevention of thrombosis, 9th ed: American College of Chest Physicians Evidence-Based Clinical Practice Guidelines. Chest. 2012 ; 141 (2 suppl). e195S - e226S
42. Kanaan AO, Silva MA, Donovan JL, Roy T, Al-Homsi AS. Meta-analysis of venous thromboembolism prophylaxis in medically Ill patients. Clin Ther. 2007 ; 29 (11). 2395-2405
43. Aldawood A, Arabi Y, Aljumah A, et al. The incidence of venous thromboembolism and practice of deep venous thrombosis prophylaxis in hospitalized cirrhotic patients. Thromb J. 2011 ; 9 (1). 1
44. Bechmann LP, Sichau M, Wichert M, Gerken G, Kröger K, Hilgard P. Low-molecular-weight heparin in patients with advanced cirrhosis. Liver Int. 2011 ; 31 (1). 75-82
45. Nguyen GC, Segev DL, Thuluvath PJ. Racial disparities in the management of hospitalized patients with cirrhosis and complications of portal hypertension: a national study. Hepatology. 2007 ; 45 (5). 1282-1289
46. La Mura V, Abraldes JG, Raffa S, et al. Prognostic value of acute hemodynamic response to i.v. propranolol in patients with cirrhosis and portal hypertension. J Hepatol. 2009 ; 51 (2). 279-287
47. Delgado MG, Seijo S, Yepes I, et al. Efficacy and safety of anticoagulation on patients with cirrhosis and portal vein thrombosis. Clin Gastroenterol Hepatol. 2012 ; 10 (7). 776-783
48. Amitrano L, Guardascione MA, Menchise A, et al. Safety and efficacy of anticoagulation therapy with low molecular weight heparin for portal vein thrombosis in patients with liver cirrhosis. J Clin Gastroenterol. 2010 ; 44 (6). 448-451
49. Senzolo M, Ferronato C, Burra P, Sartori MT. Anticoagulation for portal vein thrombosis in cirrhotic patients should be always considered. Intern Emerg Med. 2009 ; 4 (2). 161-162
50. Francoz C, Belghiti J, Vilgrain V, et al. Splanchnic vein thrombosis in candidates for liver transplantation: usefulness of screening and anticoagulation. Gut. 2005 ; 54 (5). 691-697
51. Villa E, Zecchini R, Marietta M, et al. Enoxaparin prevents portal vein thrombosis (PVT) and decompensation in advanced cirrhotic patients: final report of a prospective randomized controlled trial (abstract 120). Hepatology. 2011 ; 54 ( 418a ):
52. Sharara AI, Rockey DC. Gastroesophageal variceal hemorrhage. N Engl J Med. 2001 ; 345 (9). 669-681
53. Boks AL, Brommer EJ, Schalm SW, Van Vliet HH. Hemostasis and fibrinolysis in severe liver failure and their relation to hemorrhage. Hepatology. 1986 ; 6 (1). 79-86
54. Escorsell A, Bordas JM, Castaneda B, et al. Predictive value of the variceal pressure response to continued pharmacological therapy in patients with cirrhosis and portal hypertension. Hepatology. 2000 ; 31 (5). 1061-1067
55. Dell'era A, Bosch J. Review article: the relevance of portal pressure and other risk factors in acute gastro-oesophageal variceal bleeding. Aliment Pharmacol Ther. 2004 ; 20 (suppl 3). 8-15
56. Massicotte L, Lenis S, Thibeault L, Sassine MP, Seal RF, Roy A. Effect of low central venous pressure and phlebotomy on blood product transfusion requirements during liver transplantations. Liver Transpl. 2006 ; 12 (1). 117-123
57. Kravetz D, Sikuler E, Groszmann RJ. Splanchnic and systemic hemodynamics in portal hypertensive rats during hemorrhage and blood volume restitution. Gastroenterology. 1986 ; 90 (5 pt 1). 1232-1240
58. Castaneda B, Morales J, Lionetti R, et al. Effects of blood volume restitution following a portal hypertensive-related bleeding in anesthetized cirrhotic rats. Hepatology. 2001 ; 33 (4). 821-825
59. Garcia-Tsao G, Sanyal AJ, Grace ND, et al. Prevention and management of gastroesophageal varices and variceal hemorrhage in cirrhosis. Am J Gastroenterol. 2007 ; 102 (9). 2086-2102
60. Bosch J, Thabut D, Albillos A, et al. Recombinant factor VIIa for variceal bleeding in patients with advanced cirrhosis: a randomized, controlled trial. Hepatology. 2008 ; 47 (5). 1604-1614
61. McGill DB, Rakela J, Zinsmeister AR, Ott BJ. A 21-year experience with major hemorrhage after percutaneous liver biopsy. Gastroenterology. 1990 ; 99 (5). 1396-1400
62. Grabau CM, Crago SF, Hoff LK, et al. Performance standards for therapeutic abdominal paracentesis. Hepatology. 2004 ; 40 (2). 484-488
63. Terjung B, Lemnitzer I, Dumoulin FL, et al. Bleeding complications after percutaneous liver biopsy. An analysis of risk factors. Digestion. 2003 ; 67 (3). 138-145
64. Goulis J, Armonis A, Patch D, Sabin C, Greenslade L, Burroughs AK. Bacterial infection is independently associated with failure to control bleeding in cirrhotic patients with gastrointestinal hemorrhage. Hepatology. 1998 ; 27 (5). 1207-1212
65. Vivas S, Rodriguez M, Palacio MA, Linares A, Alonso JL, Rodrigo L. Presence of bacterial infection in bleeding cirrhotic patients is independently associated with early mortality and failure to control bleeding. Dig Dis Sci. 2001 ; 46 (12). 2752-2757
66. Bernard B, Grange JD, Khac EN, Amiot X, Opolon P, Poynard T. Antibiotic prophylaxis for the prevention of bacterial infections in cirrhotic patients with gastrointestinal bleeding: a meta-analysis. Hepatology. 1999 ; 29 (6). 1655-1661
67. Hou MC, Lin HC, Liu TT, et al. Antibiotic prophylaxis after endoscopic therapy prevents rebleeding in acute variceal hemorrhage: a randomized trial. Hepatology. 2004 ; 39 (3). 746-753
68. Montalto P, Vlachogiannakos J, Cox DJ, Pastacaldi S, Patch D, Burroughs AK. Bacterial infection in cirrhosis impairs coagulation by a heparin effect: a prospective study. J Hepatol. 2002 ; 37 (4). 463-470
69. Wanless IR, Wong F, Blendis LM, Greig P, Heathcote EJ, Levy G. Hepatic and portal vein thrombosis in cirrhosis: possible role in development of parenchymal extinction and portal hypertension. Hepatology. 1995 ; 21 (5). 1238-1247
70. Corpechot C, Barbu V, Wendum D, et al. Hypoxia-induced VEGF and collagen I expressions are associated with angiogenesis and fibrogenesis in experimental cirrhosis. Hepatology. 2002 ; 35 (5). 1010-1021
71. Duplantier JG, Dubuisson L, Senant N, et al. A role for thrombin in liver fibrosis. Gut. 2004 ; 53 (11). 1682-1687
72. Fiorucci S, Antonelli E, Distrutti E, et al. PAR1 antagonism protects against experimental liver fibrosis. Role of proteinase receptors in stellate cell activation. Hepatology. 2004 ; 39 (2). 365-375
73. Wright M, Goldin R, Hellier S, et al. Factor V Leiden polymorphism and the rate of fibrosis development in chronic hepatitis C virus infection. Gut. 2003 ; 52 (8). 1206-1210
74. Assy N, Pettigrew N, Lee SS, Chaudhary RK, Johnston J, Minuk GY. Are chronic hepatitis C viral infections more benign in patients with hemophilia?. Am J Gastroenterol. 2007 ; 102 (8). 1672-1676
75. Abe W, Ikejima K, Lang T, et al. Low molecular weight heparin prevents hepatic fibrogenesis caused by carbon tetrachloride in the rat. J Hepatol. 2007 ; 46 (2). 286-294
76. Anstee QM, Goldin RD, Wright M, Martinelli A, Cox R, Thursz MR. Coagulation status modulates murine hepatic fibrogenesis: implications for the development of novel therapies. J Thromb Haemost. 2008 ; 6 (8). 1336-1343
77. Gokturk HS, Demir M, Ozturk NA, et al. Plasma viscosity changes in patients with liver cirrhosis. South Med J. 2009 ; 102 (10). 1013-1018