Vascular Disease in Patients with Nonalcoholic Fatty Liver Disease

Seminars in Thrombosis and Hemostasis

Volumn 41, Issue 5, 2015, Pages 488-493

  Potze, Wilma ^a   Siddiqui, M Shadab ^b   Sanyal, Arun J ^b,c  

^a UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

^b VIRGINIA COMMONWEALTH UNIVERSITY   (United States)

^c VIRGINIA COMMONWEALTH UNIVERSITY   (United States)

Author keywords

cardiovascular disease; coagulation disorders; hemostasis; nonalcoholic fatty liver disease; thrombosis

Indexed keywords

BLOOD CLOTTING FACTOR 11; BLOOD CLOTTING FACTOR 7; BLOOD CLOTTING FACTOR 8; BLOOD CLOTTING FACTOR 9; C REACTIVE PROTEIN; INTERLEUKIN 6; PLASMINOGEN ACTIVATOR INHIBITOR 1; TUMOR NECROSIS FACTOR ALPHA; VON WILLEBRAND FACTOR;

ARTICLE; ATHEROSCLEROSIS; CARDIOVASCULAR DISEASE; CARDIOVASCULAR MORTALITY; CARDIOVASCULAR RISK; CORONARY ARTERY DISEASE; DEEP VEIN THROMBOSIS; DEGRANULATION; FIBROGENESIS; HEMOSTASIS; HUMAN; HYPERCOAGULABILITY; LUNG EMBOLISM; METABOLIC SYNDROME X; NONALCOHOLIC FATTY LIVER; OBESITY; PORTAL VEIN THROMBOSIS; PRIORITY JOURNAL; THROMBOCYTE ACTIVATION; THROMBOCYTE ADHESION; THROMBOCYTE COUNT; THROMBOCYTE DYSFUNCTION; THROMBOCYTE MEMBRANE; CARDIOVASCULAR DISEASES; COMPLICATION; PATHOLOGY; PHYSIOLOGY; RISK FACTOR; THROMBOSIS; VASCULAR DISEASES;

CARDIOVASCULAR DISEASES; HEMOSTASIS; HUMANS; METABOLIC SYNDROME X; NON-ALCOHOLIC FATTY LIVER DISEASE; OBESITY; RISK FACTORS; THROMBOSIS; VASCULAR DISEASES;

EID: 84937815292     PISSN: 00946176     EISSN: 10989064     Source Type: Journal    
DOI: 10.1055/s-0035-1550433     Document Type: Article

References (98)

1. Browning J.D., Szczepaniak L. S., Dobbins R., et al. Prevalence of hepatic steatosis in an urban population in the United States: impact of ethnicity. Hepatology: 2004; 40 6 1387 1395
2. Vernon G., Baranova A., Younossi Z. M. Systematic review: the epidemiology and natural history of non-alcoholic fatty liver disease and non-alcoholic steatohepatitis in adults. Aliment Pharmacol Ther: 2011; 34 3 274 285
3. Ludwig J., Viggiano T. R., McGill D. B., Oh B. J. Nonalcoholic steatohepatitis: Mayo Clinic experiences with a hitherto unnamed disease. Mayo Clin Proc: 1980; 55 7 434 438
4. Chalasani N., Younossi Z., Lavine J. E., et al. The diagnosis and management of non-alcoholic fatty liver disease: Practice Guideline by the American Association for the Study of Liver Diseases, American College of Gastroenterology, and the American Gastroenterological Association. Hepatology: 2012; 55 6 2005 2023
5. Bacon B. R., Farahvash M. J., Janney C. G., Neuschwander-Tetri B. A. Nonalcoholic steatohepatitis: an expanded clinical entity. Gastroenterology: 1994; 107 4 1103 1109
6. Matteoni C. A., Younossi Z. M., Gramlich T., Boparai N., Liu Y. C., McCullough A. J. Nonalcoholic fatty liver disease: a spectrum of clinical and pathological severity. Gastroenterology: 1999; 116 6 1413 1419
7. Adams L. A., Lymp J. F., St Sauver J., et al. The natural history of nonalcoholic fatty liver disease: a population-based cohort study. Gastroenterology: 2005; 129 1 113 121
8. Ekstedt M., Franzén L. E., Mathiesen U. L., et al. Long-term follow-up of patients with NAFLD and elevated liver enzymes. Hepatology: 2006; 44 4 865 873
9. Charlton M. R., Burns J. M., Pedersen R. A., Watt K. D., Heimbach J. K., Dierkhising R. A. Frequency and outcomes of liver transplantation for nonalcoholic steatohepatitis in the United States. Gastroenterology: 2011; 141 4 1249 1253
10. Alberti K. G., Zimmet P., Shaw J.; IDF Epidemiology Task Force Consensus Group. The metabolic syndrome--a new worldwide definition. Lancet: 2005; 366 9491 1059 1062
11. Hamaguchi M., Kojima T., Takeda N., et al. The metabolic syndrome as a predictor of nonalcoholic fatty liver disease. Ann Intern Med: 2005; 143 10 722 728
12. Marchesini G., Bugianesi E., Forlani G., et al. Nonalcoholic fatty liver, steatohepatitis, and the metabolic syndrome. Hepatology: 2003; 37 4 917 923
13. Söderberg C., Stål P., Askling J., et al. Decreased survival of subjects with elevated liver function tests during a 28-year follow-up. Hepatology: 2010; 51 2 595 602
14. Targher G., Bertolini L., Padovani R., et al. Relations between carotid artery wall thickness and liver histology in subjects with nonalcoholic fatty liver disease. Diabetes Care: 2006; 29 6 1325 1330
15. Targher G., Bertolini L., Padovani R., et al. Prevalence of nonalcoholic fatty liver disease and its association with cardiovascular disease among type 2 diabetic patients. Diabetes Care: 2007; 30 5 1212 1218
16. Targher G., Day C. P., Bonora E. Risk of cardiovascular disease in patients with nonalcoholic fatty liver disease. N Engl J Med: 2010; 363 14 1341 1350
17. Sookoian S., Pirola C. J. Non-alcoholic fatty liver disease is strongly associated with carotid atherosclerosis: a systematic review. J Hepatol: 2008; 49 4 600 607
18. Sung K. C., Wild S. H., Kwag H. J., Byrne C. D. Fatty liver, insulin resistance, and features of metabolic syndrome: relationships with coronary artery calcium in 10,153 people. Diabetes Care: 2012; 35 11 2359 2364
19. Lin Y. C., Lo H. M., Chen J. D. Sonographic fatty liver, overweight and ischemic heart disease. World J Gastroenterol: 2005; 11 31 4838 4842
20. Akabame S., Hamaguchi M., Tomiyasu K., et al. Evaluation of vulnerable coronary plaques and non-alcoholic fatty liver disease (NAFLD) by 64-detector multislice computed tomography (MSCT). Circ J: 2008; 72 4 618 625
21. Treeprasertsuk S., Leverage S., Adams L. A., Lindor K. D., St Sauver J., Angulo P. The Framingham risk score and heart disease in nonalcoholic fatty liver disease. Liver Int: 2012; 32 6 945 950
22. Musso G., Gambino R., Cassader M., Pagano G. Meta-analysis: natural history of non-alcoholic fatty liver disease (NAFLD) and diagnostic accuracy of non-invasive tests for liver disease severity. Ann Med: 2011; 43 8 617 649
23. Targher G. Relationship between high-sensitivity C-reactive protein levels and liver histology in subjects with non-alcoholic fatty liver disease. J Hepatol: 2006; 45 6 879 881, author reply 881-882
24. Targher G., Bertolini L., Rodella S., et al. NASH predicts plasma inflammatory biomarkers independently of visceral fat in men. Obesity (Silver Spring): 2008; 16 6 1394 1399
25. Hui J. M., Hodge A., Farrell G. C., Kench J. G., Kriketos A., George J. Beyond insulin resistance in NASH: TNF-alpha or adiponectin? Hepatology: 2004; 40 1 46 54
26. Jarrar M. H., Baranova A., Collantes R., et al. Adipokines and cytokines in non-alcoholic fatty liver disease. Aliment Pharmacol Ther: 2008; 27 5 412 421
27. Ozhan H., Aydin M., Yazici M., et al. Mean platelet volume in patients with non-alcoholic fatty liver disease. Platelets: 2010; 21 1 29 32
28. Shin W. Y., Jung D. H., Shim J. Y., Lee H. R. The association between non-alcoholic hepatic steatosis and mean platelet volume in an obese Korean population. Platelets: 2011; 22 6 442 446
29. Celikbilek M., Gürsoy S., Deniz K., Karaman A., Zararsiz G., Yurci A. Mean platelet volume in biopsy-proven non-alcoholic fatty liver disease. Platelets: 2013; 24 3 194 199
30. Alkhouri N., Kistangari G., Campbell C., Lopez R., Zein N. N., Feldstein A. E. Mean platelet volume as a marker of increased cardiovascular risk in patients with nonalcoholic steatohepatitis. Hepatology: 2012; 55 1 331
31. Verrijken A., Francque S., Mertens I., et al. Prothrombotic factors in histologically proven nonalcoholic fatty liver disease and nonalcoholic steatohepatitis. Hepatology: 2014; 59 1 121 129
32. Kotronen A., Joutsi-Korhonen L., Sevastianova K., et al. Increased coagulation factor VIII, IX, XI and XII activities in non-alcoholic fatty liver disease. Liver Int: 2011; 31 2 176 183
33. Tripodi A., Fracanzani A. L., Primignani M., et al. Procoagulant imbalance in patients with non-alcoholic fatty liver disease. J Hepatol: 2014; 61 1 148 154
34. Targher G., Bertolini L., Scala L., Zoppini G., Zenari L., Falezza G. Non-alcoholic hepatic steatosis and its relation to increased plasma biomarkers of inflammation and endothelial dysfunction in non-diabetic men. Role of visceral adipose tissue. Diabet Med: 2005; 22 10 1354 1358
35. Sookoian S., Castaño G. O., Burgueño A. L., et al. Circulating levels and hepatic expression of molecular mediators of atherosclerosis in nonalcoholic fatty liver disease. Atherosclerosis: 2010; 209 2 585 591
36. Thuy S., Ladurner R., Volynets V., et al. Nonalcoholic fatty liver disease in humans is associated with increased plasma endotoxin and plasminogen activator inhibitor 1 concentrations and with fructose intake. J Nutr: 2008; 138 8 1452 1455
37. Cigolini M., Targher G., Agostino G., Tonoli M., Muggeo M., De Sandre G. Liver steatosis and its relation to plasma haemostatic factors in apparently healthy men--role of the metabolic syndrome. Thromb Haemost: 1996; 76 1 69 73
38. Yener S., Akarsu M., Demir T., et al. Plasminogen activator inhibitor-1 and thrombin activatable fibrinolysis inhibitor levels in non-alcoholic steatohepatitis. J Endocrinol Invest: 2007; 30 10 810 819
39. de Larrañaga G., Wingeyer S. P., Graffigna M., et al. Plasma plasminogen activator inhibitor-1 levels and nonalcoholic fatty liver in individuals with features of metabolic syndrome. Clin Appl Thromb Hemost: 2008; 14 3 319 324
40. Barbato A., Iacone R., Tarantino G., et al. Olivetti Heart Study Research Group. Relationships of PAI-1 levels to central obesity and liver steatosis in a sample of adult male population in southern Italy. Intern Emerg Med: 2009; 4 4 315 323
41. Kargili A., Cipil H., Karakurt F., et al. Hemostatic alterations in fatty liver disease. Blood Coagul Fibrinolysis: 2010; 21 4 325 327
42. Chang M. L., Hsu C. M., Tseng J. H., et al. Plasminogen activator inhibitor-1 is independently associated with non-alcoholic fatty liver disease whereas leptin and adiponectin vary between genders. J Gastroenterol Hepatol: 2015; 30 2 329 336
43. Bilgir O., Bilgir F., Bozkaya G., Calan M. Changes in the levels of endothelium-derived coagulation parameters in nonalcoholic fatty liver disease. Blood Coagul Fibrinolysis: 2014; 25 2 151 155
44. Papatheodoridis G. V., Chrysanthos N., Cholongitas E., et al. Thrombotic risk factors and liver histologic lesions in non-alcoholic fatty liver disease. J Hepatol: 2009; 51 5 931 938
45. Assy N., Bekirov I., Mejritsky Y., Solomon L., Szvalb S., Hussein O. Association between thrombotic risk factors and extent of fibrosis in patients with non-alcoholic fatty liver diseases. World J Gastroenterol: 2005; 11 37 5834 5839
46. Tavil Y., Sen N., Yazici H. U., Hizal F., Abaci A., Cengel A. Mean platelet volume in patients with metabolic syndrome and its relationship with coronary artery disease. Thromb Res: 2007; 120 2 245 250
47. Muscari A., De Pascalis S., Cenni A., et al. Determinants of mean platelet volume (MPV) in an elderly population: relevance of body fat, blood glucose and ischaemic electrocardiographic changes. Thromb Haemost: 2008; 99 6 1079 1084
48. De Pergola G., Pannacciulli N., Coviello M., et al. sP-selectin plasma levels in obesity: association with insulin resistance and related metabolic and prothrombotic factors. Nutr Metab Cardiovasc Dis: 2008; 18 3 227 232
49. Gokulakrishnan K., Deepa R., Mohan V., Gross M. D. Soluble P-selectin and CD40L levels in subjects with prediabetes, diabetes mellitus, and metabolic syndrome--the Chennai Urban Rural Epidemiology Study. Metabolism: 2006; 55 2 237 242
50. Lee W. L., Lee W. J., Chen Y. T., et al. The presence of metabolic syndrome is independently associated with elevated serum CD40 ligand and disease severity in patients with symptomatic coronary artery disease. Metabolism: 2006; 55 8 1029 1034
51. Angelico F., Alessandri C., Ferro D., et al. Enhanced soluble CD40L in patients with the metabolic syndrome: Relationship with in vivo thrombin generation. Diabetologia: 2006; 49 6 1169 1174
52. Sobol A. B., Watala C. The role of platelets in diabetes-related vascular complications. Diabetes Res Clin Pract: 2000; 50 1 1 16
53. Murakami T., Horigome H., Tanaka K., et al. Impact of weight reduction on production of platelet-derived microparticles and fibrinolytic parameters in obesity. Thromb Res: 2007; 119 1 45 53
54. Targher G., Zoppini G., Moghetti P., Day C. P. Disorders of coagulation and hemostasis in abdominal obesity: emerging role of fatty liver. Semin Thromb Hemost: 2010; 36 1 41 48
55. Cao W., Zhao C., Shen C., Wang Y. Cytokeratin 18, alanine aminotransferase, platelets and triglycerides predict the presence of nonalcoholic steatohepatitis. PLoS ONE: 2013; 8 12 e82092
56. Sumida Y., Yoneda M., Hyogo H., et al. Japan Study Group of Nonalcoholic Fatty Liver Disease (JSG-NAFLD). A simple clinical scoring system using ferritin, fasting insulin, and type IV collagen 7S for predicting steatohepatitis in nonalcoholic fatty liver disease. J Gastroenterol: 2011; 46 2 257 268
57. Targher G., Chonchol M., Miele L., Zoppini G., Pichiri I., Muggeo M. Nonalcoholic fatty liver disease as a contributor to hypercoagulation and thrombophilia in the metabolic syndrome. Semin Thromb Hemost: 2009; 35 3 277 287
58. Northup P. G., Argo C. K., Shah N., Caldwell S. H. Hypercoagulation and thrombophilia in nonalcoholic fatty liver disease: mechanisms, human evidence, therapeutic implications, and preventive implications. Semin Liver Dis: 2012; 32 1 39 48
59. Targher G., Byrne C. D. Diagnosis and management of nonalcoholic fatty liver disease and its hemostatic/thrombotic and vascular complications. Semin Thromb Hemost: 2013; 39 2 214 228
60. Targher G., Bertolini L., Scala L., et al. Plasma PAI-1 levels are increased in patients with nonalcoholic steatohepatitis. Diabetes Care: 2007; 30 5 e31 e32
61. Meltzer M. E., Doggen C. J., de Groot P. G., Rosendaal F. R., Lisman T. Plasma levels of fibrinolytic proteins and the risk of myocardial infarction in men. Blood: 2010; 116 4 529 536
62. Westerbacka J., Kolak M., Kiviluoto T., et al. Genes involved in fatty acid partitioning and binding, lipolysis, monocyte/macrophage recruitment, and inflammation are overexpressed in the human fatty liver of insulin-resistant subjects. Diabetes: 2007; 56 11 2759 2765
63. Greco D., Kotronen A., Westerbacka J., et al. Gene expression in human NAFLD. Am J Physiol Gastrointest Liver Physiol: 2008; 294 5 G1281 G1287
64. Sookoian S., Gianotti T. F., Rosselli M. S., Burgueño A. L., Castaño G. O., Pirola C. J. Liver transcriptional profile of atherosclerosis-related genes in human nonalcoholic fatty liver disease. Atherosclerosis: 2011; 218 2 378 385
65. Northup P. G., Sundaram V., Fallon M. B., et al. Coagulation in Liver Disease Group. Hypercoagulation and thrombophilia in liver disease. J Thromb Haemost: 2008; 6 1 2 9
66. Sanyal A. J., Banas C., Sargeant C., et al. Similarities and differences in outcomes of cirrhosis due to nonalcoholic steatohepatitis and hepatitis C. Hepatology: 2006; 43 4 682 689
67. Lisman T., Bakhtiari K., Pereboom I. T., Hendriks H. G., Meijers J. C., Porte R. J. Normal to increased thrombin generation in patients undergoing liver transplantation despite prolonged conventional coagulation tests. J Hepatol: 2010; 52 3 355 361
68. 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
69. Gatt A., Riddell A., Calvaruso V., Tuddenham E. G., Makris M., Burroughs A. K. Enhanced thrombin generation in patients with cirrhosis-induced coagulopathy. J Thromb Haemost: 2010; 8 9 1994 2000
70. Sogaard K. K., Horváth-Puhó E., Gronbaek H., Jepsen P., Vilstrup H., Sorensen H. T. Risk of venous thromboembolism in patients with liver disease: a nationwide population-based case-control study. Am J Gastroenterol: 2009; 104 1 96 101
71. Northup P. G., McMahon M. M., Ruhl A. P., et al. Coagulopathy does not fully protect hospitalized cirrhosis patients from peripheral venous thromboembolism. Am J Gastroenterol: 2006; 101 7 1524 1528, quiz 1680
72. 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
73. García-Fuster M. J., Abdilla N., Fabiá M. J., Fernández C., Oliver V.; Forner M J. Venous thromboembolism and liver cirrhosis [in Spanish]. Rev Esp Enferm Dig: 2008; 100 5 259 262
74. Wu H., Nguyen G. C. Liver cirrhosis is associated with venous thromboembolism among hospitalized patients in a nationwide US study. Clin Gastroenterol Hepatol: 2010; 8 9 800 805
75. Tripodi A., Anstee Q. M., Sogaard K. K., Primignani M., Valla D. C. Hypercoagulability in cirrhosis: causes and consequences. J Thromb Haemost: 2011; 9 9 1713 1723
76. Lisman T., Kamphuisen P. W., Northup P. G., Porte R. J. Established and new-generation antithrombotic drugs in patients with cirrhosis - possibilities and caveats. J Hepatol: 2013; 59 2 358 366
77. Potze W., Porte R. J., Lisman T. Management of coagulation abnormalities in liver disease. Expert Rev Gastroenterol Hepatol: 2015; 9 1 103 114
78. Abad Rico J. I., Llau Pitarch J. V., Rocha E. Overview of venous thromboembolism. Drugs: 2010; 70 02 3 10
79. Stein P. D., Goldman J. Obesity and thromboembolic disease. Clin Chest Med: 2009; 30 3 489 493, viii viii
80. Borch K. H., Braekkan S. K., Mathiesen E. B., et al. Abdominal obesity is essential for the risk of venous thromboembolism in the metabolic syndrome: the Tromso study. J Thromb Haemost: 2009; 7 5 739 745
81. Di Minno M. N., Tufano A., Rusolillo A., Di Minno G., Tarantino G. High prevalence of nonalcoholic fatty liver in patients with idiopathic venous thromboembolism. World J Gastroenterol: 2010; 16 48 6119 6122
82. Stine J. G., Shah N. L., Argo C. K., Pelletier S., Caldwell S. H., Northup P. G. Increased risk of portal vein thrombosis in non-alcoholic steatohepatitis (NASH) and cryptogenic cirrhosis: evidence for a thrombophilic state. Hepatology: 2014; 60 1 392A 293A
83. Anstee Q. M., Dhar A., Thursz M. R. The role of hypercoagulability in liver fibrogenesis. Clin Res Hepatol Gastroenterol: 2011; 35 8-9 526 533
84. 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
85. Papatheodoridis G. V., Papakonstantinou E., Andrioti E., et al. Thrombotic risk factors and extent of liver fibrosis in chronic viral hepatitis. Gut: 2003; 52 3 404 409
86. Poujol-Robert A., Boëlle P. Y., Poupon R., Robert A. Factor V Leiden as a risk factor for cirrhosis in chronic hepatitis C. Hepatology: 2004; 39 4 1174 1175
87. Poujol-Robert A., Rosmorduc O., Serfaty L., Coulet F., Poupon R., Robert A. Genetic and acquired thrombotic factors in chronic hepatitis C. Am J Gastroenterol: 2004; 99 3 527 531
88. Anstee Q. M., Goldin R. D., Wright M., Martinelli A., Cox R., Thursz M. R. Coagulation status modulates murine hepatic fibrogenesis: implications for the development of novel therapies. J Thromb Haemost: 2008; 6 8 1336 1343
89. Wanless I. R., Belgiorno J., Huet P. M. Hepatic sinusoidal fibrosis induced by cholesterol and stilbestrol in the rabbit: 1. Morphology and inhibition of fibrogenesis by dipyridamole. Hepatology: 1996; 24 4 855 864
90. Abdel-Salam O. M., Baiuomy A. R., Ameen A., Hassan N. S. A study of unfractionated and low molecular weight heparins in a model of cholestatic liver injury in the rat. Pharmacol Res: 2005; 51 1 59 67
91. 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
92. Duplantier J. G., Dubuisson L., Senant N., et al. A role for thrombin in liver fibrosis. Gut: 2004; 53 11 1682 1687
93. Fujita K., Nozaki Y., Wada K., et al. Effectiveness of antiplatelet drugs against experimental non-alcoholic fatty liver disease. Gut: 2008; 57 11 1583 1591
94. Kopec A. K., Joshi N., Towery K. L., et al. Thrombin inhibition with dabigatran protects against high-fat diet-induced fatty liver disease in mice. J Pharmacol Exp Ther: 2014; 351 2 288 297
95. Joshi N., Kopec A. K., O'Brien K. M., et al. Coagulation-driven platelet activation reduces cholestatic liver injury and fibrosis in mice. J Thromb Haemost: 2015; 13 1 57 71
96. Luyendyk J. P., Kassel K. M., Allen K., et al. Fibrinogen deficiency increases liver injury and early growth response-1 (Egr-1) expression in a model of chronic xenobiotic-induced cholestasis. Am J Pathol: 2011; 178 3 1117 1125
97. Kodama T., Takehara T., Hikita H., et al. Thrombocytopenia exacerbates cholestasis-induced liver fibrosis in mice. Gastroenterology: 2010; 138 7 2487 2498, 2498.e1-2498.e7
98. Lisman T. Platelets and fibrin in progression of liver disease: friends or foes? J Thromb Haemost: 2015; 13 1 54 56