Preview

General Reanimatology

Advanced search

Liver Disease and Hemostasis (Review) Part 2. Cholestatic Liver Disease and Hemostasis

https://doi.org/10.15360/1813-9779-2019-6-80-93

Abstract

The presence or development of liver disorders can significantly complicate the course of critical illness and terminal conditions. Systemic hemostatic disorders are common in Intensive Care Units patients with cholestatic liver diseases, so the study of the mechanisms of their development can contribute to the understanding of the development of multiorgan failure in critical illness.

The review discusses current data on changes in hemostatic parameters in patients with cholestatic liver diseases, proposes a mechanism for the development of such disorders, which involve interactions of phospholipids with platelet and endotheliocyte membranes. It is suggested that a trend for thrombosis in patients with cholestatic liver disease is due to increased accumulation of bile acids in the systemic circulation. Available data demonstrate that the antiphospholipid syndrome may predispose to the formation of blood clots due to alterations of phospholipid composition of membranes of platelets and vascular endothelial cells by circulating antiphospholipid antibodies. Clarifying the mechanisms contributing to changes of the blood coagulation system parameters in liver disorders will aid to development of optimal correction of hemostatic disorders in patients with chronic liver diseases.

About the Authors

Vasiliy I. Reshetnyak
A. I. Evdokimov Moscow State University of medicine and dentistry, Ministry of Health of Russia
Russian Federation
20 Delegatskaya Str., Build 1, 127473 Moscow


Igor V. Maev
A. I. Evdokimov Moscow State University of medicine and dentistry, Ministry of Health of Russia
Russian Federation
20 Delegatskaya Str., Build 1, 127473 Moscow


Tatiana M. Reshetnyak
V. A. Nasonova Research Institute of Rheumatology
Russian Federation
34A Kashirskoye highway, Moscow 115522


Sergei V. Zhuravel
N. V. Sklifosovsky Research Institute of Emergency Care, Moscow Healthcare Department
Russian Federation
3 Bolshaya Sukharevskaya Square, Moscow 129090


Vladimir M. Pisarev
V. A. Negovsky Research Institute of General Reanimatology, Federal Research and Clinical Center of Intensive Care Medicine and Rehabilitology
Russian Federation
25 Petrovka Str., Build. 2, 107031 Moscow


References

1. Batyrova А.S., Bakanov M.I., Surkov А.N. Modern views on the hemostatic system in chronic liver diseases (literature review). Klinicheskaya laboratornaya diagnostika 2015; 60 (8): 40–44 [In Russ.]

2. Reshetnyak V.I., Maev I.V., Reshetnyak T.M., Zhuravel S.V., Pisarev V.M. Liver Diseases and the Hemostasis (Rewiew) Part 1. Non-Cholestatic Diseases of the Liver and Hemostasis. Obshchaya Reanimatologiya=General Reanimatology. 2019; 15 (5): 74–87. [In Russ.] DOI: 10.15360/1813-9779-2019-5-74-87.

3. Intagliata N.M., Caldwell S.H. Changes in hemostasis in liver disease. J. Hepatol. 2017 Dec; 67 (6): 1332–1333. DOI: 10.1016/j.jhep.2017.07.001. PMID: 29156209.

4. Tripodi A. Hemostasis in Acute and Chronic Liver Disease. Semin Liver Dis. 2017; 37 (1): 28–32. DOI: 10.1055/s-0036-1597770. PMID: 28201846

5. Flores B., Trivedi H.D., Robson S.C., Bonder A. Hemostasis, bleeding and thrombosis in liver disease. J Transl. Sci. 2017; 3 (3). DOI: 10.15761/JTS.1000182. PMID: 30221012

6. Minov А.F., Dzyadzko А.M., Rummo O.O. Violation of hemostasis in liver diseases. Vestnik transplantalogii i iskusstvennykh organov. 2010; 2 (12): 82–91 [In Russ.]

7. Morozov Yu.A., Mednikov R.V., Charnaya M.A. Violations of the hemostatic system in liver pathology and their diagnosis. Gemorragicheskie diatezy, trombozy, trombofilii. 2014; 1: 162–174 [In Russ.]

8. Sira J., Eyre L. Physiology of Hemostasis. Anaesthesia & Intensive Care Medicine. 2016; 17 (2): 79–82

9. Beuers U., Gershwin M.E., Gish R.G., Invernizzi P., Jones D.E., Lindor K., Ma X., Mackay I.R., Parés A., Tanaka A., Vierling J.M., Poupon R. Changing nomenclature for PBC: From ‘cirrhosis’ to ‘cholangitis’. Hepatology 2015; 62: 1620–1622. DOI: 10.1002/hep.28140. PMID: 26372460

10. Reshetnyak V.I. Concept on the pathogenesis and treatment of primary biliary cirrhosis. World J Gastroenterol. 2006; 12: 7250–7262. DOI: 10.3748/wjg.v12.i45.7250. PMID: 17143938

11. Reshetnyak V.I. Primary biliary cirrhosis: clinical and laboratory criteria for its diagnosis. World J Gastroenterol 2015; 21: 7683–7708. DOI: 10.3748/wjg.v21.i25.7683. PMID: 26167070

12. Gerussi A., Cristoferi L., Carbone M., Asselta R., Invernizzi P. The immunobiology of female predominance in primary biliary cholangitis. Journal of Autoimmunity 2018; 95: 124–132. DOI: 10.1016/j.jaut. 2018.10.015. PMID: 30509386

13. Lindor K.D., Bowlus C.L., Boyer J., Levy C., Mayo M. Primary Biliary Cholangitis: 2018 Practice Guidance from the American Association for the Study of Liver Diseases. Hepatology. 2018 Aug 2. DOI: 10.1002/hep.30145. PMID: 30070375

14. Ueda Y., Kaido T., Okajima H., Hata K., Anazawa T., Yoshizawa A., Yagi S., Taura K., Masui T., Yamashiki N., Haga H., Nagao M., Marusawa H., Seno H., Uemoto S. Long-term prognosis and recurrence of primary sclerosing cholangitis after liver transplantation: a single-center experience. Transplant Direct 2017; 3: e334. DOI: 10.1097/TXD.0000000000000751. PMID: 29536035

15. Tugushev А.S. Liver cirrhosis and thrombosis. Zaporozhskij meditsinskij zhurnal. 2010; 3 (12): 78–83. [In Russ.]

16. Kozlovskij V.I., Kovtun O.S., Seroukhova O.P., Detkovskaya I.N., Kozlovskij I.V. Research methods and clinical significance of platelet aggregation. Focus on spontaneous aggregation. Vestnik VGMU. 2013; 3: 79–91. [In Russ.]

17. Gores G.J., Wiesner R.H., Dickson E.R., Zinsmeister A.R., Jorgensen R.A., Langworthy A. Prospective evaluation of esophageal varices in primary biliary cirrhosis: development, natural history and influence on survival. Gastroenterology 1989; 96: 1552–1559. DOI: 10.1016/0016-5085 (89)90526-X. PMID: 2785470

18. Biagini M.R., Guardascione M., McCormick A.P., Raskino C., McIntyre N., Burroughs A.K. Bleeding varices in PBC and its prognostic significance. Gut 1990; 31: A1209. DOI: 10.1016/0168-8278 (90)91361-Y

19. Yang L., Rezaie A.R. Calcium-binding sites of the thrombin-thrombomodulin-protein C complex: possible implications for the effect of platelet factor 4 on the activation of vitamin K-dependent coagulation factors. Thromb Haemost. 2007; 97 (6): 899–906. PMID: 17549291

20. Agarwal S., Joyner K.A. Jr, Swaim M.W. Ascites fluid as a possible origin for hyperfibrinolysis in advanced liver disease. Am J Gastroenterol 2000; 95: 3218–3224. DOI: 10.1111/j.1572-0241.2000.03299.x. PMID: 11095345

21. Ben-Ari Z., Panagou M., Patch D., Bates S., Osman E., Pasi J., Burroughs A. Hypercoagulability in patients with primary biliary cirrhosis and primary sclerosing cholangitis evaluated by thrombelastography. J Hepatol 1997; 26: 554–559. DOI: 10.1016/S0168-8278 (97)80420-5. PMID: 9075662

22. Pihusch R., Rank A., Göhring P., Pihusch M., Hiller E., Beuers U. Platelet function rather than plasmatic coagulation explains hypercoagulable state in cholestatic liver disease. J. Hepatol 2002; 37: 548–555. DOI: 10.1016/S0168-8278 (02)00239-8. PMID: 12399218

23. Sullivan B.P., Weinreb P.H., Violette S.M., Luyendyk J.P. The coagulation system contributes to alphaVbeta6-integrin expression and liver fibrosis induced by cholestasis. Am. J. Pathol 2010; 177: 2837–2849. DOI: 10.2353/ajpath.2010.100425. PMID: 21037076

24. Joshi N., Kopec A.K., O’Brien K.M., Towery K.L., Cline-Fedewa H., Williams K.J, Copple B.L., Flick M.J., Luyendyk J.P. Coagulation-driven platelet activation reduces cholestatic liver injury and fibrosis in mice. J. Thromb. Haemost. 2015; 13: 57–71. DOI: 10.1111/jth.12770. PMID: 25353084

25. Hartmann M., Szalai C., Saner F.H. Hemostasis in liver transplantation: Pathophysiology, monitoring, and treatment. World J. Gastroenterol. 2016; 22 (4): 1541–1550. DOI: 10.3748/wjg.v22.i4.1541. PMID: 26819521

26. Krzanicki D., Sugavanam A., Mallett S. Intraoperative hypercoagulability during liver transplantation as demonstrated by thromboelastography. Liver Transpl. 2013; 19 (8): 852–861. DOI: 10.1002/lt.23668. PMID: 23696318

27. Francis J.L., Armstrong D.J. Fibrinogen-bound sialic acid levels in the dysfibrinogenaemia of liver disease. Haemostasis 1982; 11: 215–222. DOI: 10.1159/000214666. PMID: 6290353

28. Dumitrescu G., Januszkiewicz A., Ågren A., Magnusson M., Wahlin S., Wernerman J. Thrombelastometry: relation to the severity of liver cirrhosis in patients considered for liver transplantation. Medicine (Baltimore) 2017; 96: e7101. DOI: 10.1097/MD.0000000000007101. PMID: 28591054

29. Shaydakov M.E., Blebea J. Thromboelastography (TEG). StatPearls [Internet]. Treasure Island (FL): StatPearls Publishing; 2019. PMID: 30725746

30. Mannucci P.M., Vigano S. Deficiencies of protein C, an inhibitor of blood coagulation. Lancet 1982; 2: 463–467. DOI: 10.1016/S0140-6736 (82)90494-9. PMID: 6125639

31. Reshetnyak V.I. Physiological and molecular biochemical mechanisms of bile formation. World J Gastroenterol 2013; 19: 7341–7360. DOI: 10.3748/wjg.v19.i42.7341. PMID: 24259965

32. Mooberry M.J., Key N.S. Microparticle analysis in disorders of hemostasis and thrombosis. Cytometry A. 2016; 89 (2): 111–122. DOI: 10.1002/cyto.a.22647. PMID: 25704723

33. Morel O., Jesel L., Freyssinet J.M., Toti F. Cellular mechanisms underlying the formation of circulating microparticles. Arterioscler. Thromb. Vasc. Biol. 2011; 31 (1): 15–26. DOI: 10.1161/ATVBAHA.109.200956. PMID: 21160064

34. Key N.S., Mackman N. Tissue factor and its measurement in whole blood, plasma, and microparticles. Semin. Thromb. Hemost. 2010; 36 (8): 865–875. DOI: 10.1055/s-0030-1267040. PMID: 21049387

35. Owens A.P. 3rd, Mackman N. Microparticles in hemostasis and thrombosis. Circ Res. 2011; 108 (10): 1284–1297. DOI: 10.1161/CIRCRESAHA.110.233056. PMID: 21566224

36. Horstman L.L., Jy W., Jimenez J.J., Bidot C., Ahn Y.S. New horizons in the analysis of circulating cell-derived microparticles. Keio J. Med. 2004; 53 (4): 210–230. PMID: 15647627

37. Sinauridze E.I., Kireev D.A., Popenko N.Y., Pichugin A.V., Panteleev M.A., Krymskaya O.V., Ataullakhanov F.I. Platelet microparticle membranes have 50- to 100-fold higher specific procoagulant activity than activated platelets. Thromb. Haemost. 2007; 97 (3): 425–434. PMID: 17334510

38. Northup P.G., Caldwell S.H. Coagulation in liver disease: a guide for the clinician. Clin Gastroenterol. Hepatol. 2013; 11 (9): 1064–1074. PMID: 23506859

39. Harrison M.F. The Misunderstood Coagulopathy of Liver Disease: A Review for the Acute Setting. West J. Emerg Med. 2018; 19 (5): 863–871. DOI: 10.5811/westjem.2018.7.37893. PMID: 30202500

40. Witters P., Freson K., Verslype C., Peerlinck K., Hoylaerts M., Nevens F., Van Geet C., Cassiman D. Review article: blood platelet number and function in chronic liver disease and cirrhosis. Aliment Pharmacol Ther. 2008; 27 (11): 1017–1029. DOI: 10.1111/j.1365-2036.2008.03674.x. PMID: 18331464

41. Carbone M., Neuberger J. Liver transplantation in PBC and PSC: indications and disease recurrence. Clin Res Hepatol Gastroenterol 2011; 35: 446-454. DOI: 10.1016/j.clinre.2011.02.007. PMID: 21459072

42. Pena Polanco N.A, Levy C., Martin E.F. Cholestatic liver diseases after liver transplant. Clin Liver Dis 2017; 21: 403–420. DOI: 10.1016/j.cld.2016.12.011. PMID: 28364821

43. Martin E.F., Levy C. Timing, management, and outcomes of liver transplantation in primary sclerosing cholangitis. Semin. Liver Dis. 2017; 37: 305–313. DOI: 10.1055/s-0037-1608655. PMID: 29272893

44. She W.H., Chan A.C.Y., Cheung T.T., Lo C.M., Chok K.S.H. Survival outcomes of liver transplantation for hepatocellular carcinoma in patients with normal, high and very high preoperative alpha-fetoprotein levels. World J. Hepatol. 2018; 10 (2): 308–318. DOI: 10.4254/wjh.v10.i2.308. PMID: 29527266

45. Carbone M., Neuberger J.M. Autoimmune liver disease, autoimmunity and liver transplantation. J. Hepatol. 2014; 60 (1): 210–223. DOI: 10.1016/j.jhep.2013.09.020. PMID: 24084655

46. Cruz-Ramón V., Chinchilla-López P., Ramírez-Pérez O., MéndezSánchez N. Effects of portal vein thrombosis on the outcomes of liver cirrhosis: a Mexican perspective. J Transl Int Med 2017; 5: 189–191. DOI: 10.1515/jtim-2017-0031. PMID: 29340273

47. Trebicka J., Strassburg C.P. Etiology and complications of portal vein thrombosis. Viszeralmedizin 2014; 30: 375–380. DOI: 10.1159/000369987. PMID: 26288604

48. Primignani M., La Mura V. Diagnosis of thrombophilia/prothrombotic conditions in patients with liver disease. Clin Liver Dis 2014; 6: 126–128. DOI: 10.1002/cld.342

49. Saugel B., Lee M., Feichtinger S., Hapfelmeier A., Schmid R.M., Siveke J.T. Thrombophilic factor analysis in cirrhotic patients with portal vein thrombosis. J. Thromb. Thrombolysis 2015; 40: 54–60. DOI: 10.1007/s11239-014-1124-z. PMID: 25115839

50. Amitrano L., Brancaccio V., Guardascione M.A., Margaglione M., Iannaccone L., D’Andrea G., Marmo R., Ames P.R., Balzano A. Inherited coagulation disorders in cirrhotic patients with portal vein thrombosis. Hepatology 2000; 31: 345–348. DOI: 10.1002/hep.510310213. PMID: 10655256

51. Dentali F., Galli M., Gianni M., Ageno W. Inherited thrombophilic abnormalities and risk of portal vein thrombosis. A meta-analysis. Thromb. Haemost 2008; 99: 675–682. DOI: 10.1160/TH07-08-0526. PMID: 18392325

52. Muciño-Bermejo J., Carrillo-Esper R., Uribe M., Méndez-Sánchez N. Coagulation abnormalities in the cirrhotic patient. Ann. Hepatol 2013; 12: 713–724. PMID: 24018489

53. Tripodi A., Primignani M., Lemma L., Chantarangkul V., Mannucci P.M. Evidence that low protein C contributes to the procoagulant imbalance in cirrhosis. J. Hepatol 2013; 59: 265–270. DOI: 10.1016/j.jhep. 2013.03.036. PMID: 23583273

54. Manzano-Robleda Mdel C., Barranco-Fragoso B., Uribe M., MéndezSánchez N. Portal vein thrombosis: what is new? Ann. Hepatol 2015; 14: 20–27. PMID: 25536638

55. Reshetnyak T.M., Shcherbakova M.Yu., Zhdanova L.V., Nasonov E.L. Antiphospholipid syndrome, antiphospholipid antibodies and genetic thrombophilia in children with somatic pathology. Nauchnoprakticheskaya revmatologiya. 2008; 4: 48–57. [In Russ.]

56. Bezemer I.D., van der Meer F.J., Eikenboom J.C., Rosendaal F.R., Doggen C.J. The value of family history as a risk indicator for venous thrombosis. Arch. Intern. Med. 2009; 169: 610–615. DOI: 10.1001/archinternmed.2008.589. PMID: 19307525

57. Postnov A.Yu., Goncharova L.N., Hasanova Z.B., Birlyukova D.V., Konovalova N.V., Timoshkina E.I., Semenova S.V., Snegovskoj V.A., Kuzovenkova O.N. The study of genetic markers of thrombosis in individuals with arterial hypertension in the titular population of the Republic of Mordovia. Arkhiv patologii. 2009; 71 (4): 34–36 [In Russ.]

58. Reshetnyak T.M. Antiphospholipid syndrome: diagnosis and clinical manifestations (lecture) Nauchno-prakticheskaya revmatologiya. 2014; 52 (1): 56–71. [In Russ.] DOI: 10.14412/1995-4484-2014-56-71

59. Shafia S., Zargar M.H., Khan N., Ahmad R., Shah Z.A., Asimi R. High prevalence of factor V Leiden and prothrombin G20101A mutations in Kashmiri patients with venous thromboembolism. Gene 2018; 654: 1–9. DOI: 10.1016/j.gene.2018.02.031. PMID: 29454086

60. Ferro D., Quintarelli C., Lattuada A., Leo R., Alessandroni M., Mannucci P.M., Violi F. High plasma levels of von Willebrand factor as a marker of endothelial perturbation in cirrhosis: relationship to endotoxemia. Hepatology 1996; 23: 1377–1383. DOI: 10.1002/hep.510230613. PMID: 8675154

61. Tripodi A., Anstee Q.M., Sogaard K.K., Primignani M., Valla D.C. Hypercoagulability in cirrhosis: causes and consequences. J. Thromb. Haemost. 2011; 9: 1713–1723. DOI: 10.1111/j.1538-7836.2011.04429.x. PMID: 21729237

62. Miyakis S., Lockshin M.D., Atsumi T., Branch D.W., Brey R.L., Cervera R., Derksen R.H., DE Groot P.G., Koike T., Meroni P.L., Reber G., Shoenfeld Y., Tincani A., Vlachoyiannopoulos P.G., Krilis S.A. International consensus statement on an update of the preliminary classification criteria for antiphospholipid syndrome (APS). J. Thromb. Haemost. 2006; 4: 295–306. DOI: 10.1111/j.1538-7836.2006.01753.x. PMID: 16420554

63. Nasonov E.L. Antiphospholipid syndrome. М.: Littera, 2004: 440. [In Russ.] ISBN: 5-98216-010-5

64. Erkan D., Pierangeli S.S., editors. Antiphospholipid syndrome: insights and highlights from the 13th International Congress on Antiphospholipid Antibodies. New York: Springer Science+Business Media, 2012: 23–113. ISBN: 9781461431947

65. Asherson R.A., Cervera R., Piette J-Ch., Shoenfeld Y., editors. The antiphospholipid syndrome II: autoimmune thrombosis. New York: Elsevier, 2002: 478. ISBN: 9780080527307

66. Reshetnyak T.M., Vavilova T.V. Clinical and laboratory criteria for the diagnosis of antiphospholipid syndrome — what is important for a practical doctor to know (lecture). Klinicheskaya laboratornaya diagnostika. [in Russ.] 2010; 11: 13–20.

67. Reshetnyak T.M. Chapter 13. Antiphospholipid syndrome. 377-406. In the book. Badokin V.V., ed. Rheumatology. Clinical lectures. M.: Litter, 2012: 592. [In Russ.] ISBN: 978-5-4235-0062-7.

68. Willis R., Pierangeli S.S. Pathophysiology of the antiphospholipid antibody syndrome. Auto Immun. Highlights 2011; 2: 35–52. DOI: 10.1007/s13317-011-0017-9. PMID: 26000118

69. Willis R., Gonzalez E.B., Brasier A.R. The journey of antiphospholipid antibodies from cellular activation to antiphospholipid syndrome. Curr. Rheumatol Rep 2015; 17: 16. DOI: 10.1007/s11926-014-0485-9. PMID: 25761923

70. Cervera R., Piette J.C., Font J., Khamashta M.A., Shoenfeld Y., Camps M.T., Jacobsen S., Lakos G., Tincani A., Kontopoulou-Griva I., Galeazzi M., Meroni P.L., Derksen R.H., de Groot P.G., Gromnica-Ihle E., Baleva M., Mosca M., Bombardieri S., Houssiau F., Gris J.C., Quéré I., Hachulla E., Vasconcelos C., Roch B., Fernández-Nebro A., Boffa M.C., Hughes G.R., Ingelmo M.; Euro-Phospholipid Project Group. Antiphospholipid syndrome: clinical and immunologic manifestations and patterns of disease expression in a cohort of 1,000 patients. Arthritis Rheum. 2002; 46: 1019–1027. DOI: 10.1002/art.10187. PMID: 11953980

71. Mackworth-Young C.G., Melia W.M., Harris E.N., Gharavi A.E., Sivathondan Y., Derue G., Sherlock S., Hughes G.R. The Budd-Chiari syndrome. Possible pathogenic role of anti-phospholipid antibodies. J. Hepatol. 1986; 3: 83–86. DOI: 10.1016/S0168-8278 (86)80150-7. PMID: 3091679

72. Uthman I., Khamashta M. The abdominal manifestations of the antiphospholipid syndrome. Rheumatology (Oxford) 2007; 46: 1641–1647. DOI: 10.1093/rheumatology/kem158. PMID: 17636180

73. Reshetnyak T.M., Seredavkina N.V., Satybaldyeva M.A., Nasonov E.L., Reshetnyak V.I. Liver transplantation in a patient with primary antiphospholipid syndrome and Budd-Chiari syndrome. World J. Hepatol. 2015; 7: 2229–2236. DOI: 10.4254/wjh.v7.i19.2229. PMID: 26380049

74. Hefaiedh R., Cheikh M., Marsaoui L., Ennaifer R., Romdhane H., Ben Nejma H., Bel Hadj N., Arfa N., Khalfallah M.T. The Budd-Chiari syndrome. Tunis Med 2013; 91: 376–381. PMID: 23868034

75. Goel R.M., Johnston E.L., Patel K.V., Wong T. Budd-Chiari syndrome: investigation, treatment and outcomes. Postgrad Med J 2015; 91: 692–697. DOI: 10.1136/postgradmedj-2015-133402. PMID: 26494427

76. Valla D.C. Budd-Chiari syndrome/hepatic venous outflow tract obstruction. Hepatol Int 2018; 12 Suppl 1: 168–180. DOI: 10.1007/ s12072-017-9810-5. PMID: 28685257

77. Aggarwal R., Ravishankar B., Misra R., Aggarwal A., Dwivedi S., Naik S.R. Significance of elevated IgG anticardiolipin antibody levels in patients with Budd-Chiari syndrome. Am. J. Gastroenterol. 1998; 93: 954–957. DOI: 10.1111/j.1572-0241.1998.00286.x. PMID: 9647027

78. Espinosa G., Font J., García-Pagan J.C., Tàssies D., Reverter J.C., Gaig C., Cervantes F., Cervera R., Bosch J., Ingelmo M. Budd-Chiari syndrome secondary to antiphospholipid syndrome: clinical and immunologic characteristics of 43 patients. Medicine (Baltimore) 2001; 80: 345–354. DOI: 10.1097/00005792-200111000-00001. PMID: 11704712

79. Mansuco A. Budd-Chiari syndrome management: lights and shadows. World J. Hepatol. 2011; 3: 262–264. DOI: 10.4254/wjh.v3.i10.262. PMID: 22059108

80. Bhattacharyya M., Makharia G., Kannan M., Ahmed R.P., Gupta P.K., Saxena R. Inherited prothrombotic defects in Budd-Chiari syndromeand portal vein thrombosis: a study from North India. Am. J. Clin. Pathol. 2004; 121: 844–847. DOI: 10.1309/F2U1-XBV4-RXYU-AYG0. PMID: 15198356

81. Remkova A. Diagnostic approach to hypercoagulable states. Bratisl Lek Listy 2006; 107: 292–295. PMID: 17125064

82. Lian E.C., Tzakis A.G., Andrews D. Response of factor V inhibitor to rituximab in a patient who received liver transplantation for primary biliary cirrhosis. Am J Hematol 2004; 77: 363–365. DOI: 10.1002/ajh.20181. PMID: 15551286

83. Lisman T., Caldwell S.H., Burroughs A.K., Northup P.G., Senzolo M., Stravitz R.T., Tripodi A., Trotter J.F., Valla D.C., Porte R.J. Coagulation in Liver Disease Study Group. Hemostasis and thrombosis in patients with liver disease: the ups and downs. J Hepatol 2010; 53: 362–371. DOI: 10.1016/j.jhep.2010.01.042. PMID: 20546962

84. Lisman T., Porte R.J. Rebalanced hemostasis in patients with liver disease: evidence and clinical consequences. Blood 2010; 116: 878–885. DOI: 10.1182/blood-2010-02-261891. PMID: 20400681

85. Reshetnyak V.I., Zhuravel S.V., Kuznetsova N.K., Pisarev V.М., Klychnikova E.V., Syutkin V.Е., Reshetnyak Т.M. The System of Blood Coagulation in Normal and in Liver Transplantation (Review). Obshchaya Reanimatologiya=General Reanimatology. 2018; 14 (5): 58-84. [In Russ.] DOI: 10.15360/1813-9779-2018-5-58-84


Review

For citations:


Reshetnyak V.I., Maev I.V., Reshetnyak T.M., Zhuravel S.V., Pisarev V.M. Liver Disease and Hemostasis (Review) Part 2. Cholestatic Liver Disease and Hemostasis. General Reanimatology. 2019;15(6):80-93. https://doi.org/10.15360/1813-9779-2019-6-80-93

Views: 1857


Creative Commons License
This work is licensed under a Creative Commons Attribution 4.0 License.


ISSN 1813-9779 (Print)
ISSN 2411-7110 (Online)