Etiopathogenesis, Prevention, and Treatment of Thromboembolism in Inflammatory Bowel Disease

Clinical and Applied Thrombosis/Hemostasis

Volumn 23, Issue 6, 2017, Pages 501-510

  Alkim, Huseyin ^a   Koksal, Ali Riza ^a   Boga, Salih ^a   Sen, Ilker ^a   Alkim, Canan ^a  

^a II Ear Nose Throat Head and Neck Surgery   (Turkey)

Author keywords

hypercoagulability; inflammatory bowel disease; low molecular weight heparins; thrombophilia; thrombosis; thrombosis prophylaxis

Indexed keywords

5,10 METHYLENETETRAHYDROFOLATE REDUCTASE (FADH2); AZATHIOPRINE; CORTICOSTEROID; CYCLOSPORIN; HEPARIN; METHOTREXATE; LOW MOLECULAR WEIGHT HEPARIN;

ADULT; ARTICLE; DEEP VEIN THROMBOSIS; GENE; HUMAN; HYPERCOAGULABILITY; HYPERHOMOCYSTEINEMIA; INFLAMMATORY BOWEL DISEASE; LUNG EMBOLISM; META ANALYSIS (TOPIC); MTHFR GENE; PRIORITY JOURNAL; RHEUMATOID ARTHRITIS; RISK FACTOR; THROMBOEMBOLISM; THROMBOSIS; COMPLICATION; PREMEDICATION; PROCEDURES; VENOUS THROMBOEMBOLISM;

HEPARIN, LOW-MOLECULAR-WEIGHT; HUMANS; INFLAMMATORY BOWEL DISEASES; PREMEDICATION; VENOUS THROMBOEMBOLISM;

EID: 85027573453     PISSN: 10760296     EISSN: 19382723     Source Type: Journal    
DOI: 10.1177/1076029616632906     Document Type: Article

References (75)

1. Yoshida H, Granger DN,. Inflammatory bowel disease: a paradigm for the link between coagulation and inflammation. Inflamm Bowel Dis. 2009; 15 (8): 1245-1255.
2. Bargen JA, Barker NW,. Extensive arterial and venous thrombosis complicating chronic ulcerative colitis. Arch Intern Med. 1936; 58: 17-31.
3. Tan VP, Chung A, Yan BP, Gibson PR,. Venous and arterial disease in inflammatory bowel disease. J Gastroenterol Hepatol. 2013; 28 (7): 1095-1113.
4. Tezel A, Demir M,. Inflammatory bowel disease and thrombosis. Turk J Hematol. 2012; 29 (2): 111-119.
5. Koutroumpakis EI, Tsiolakidou G, Koutroubakis IE,. Risk of venous thromboembolism in patients with inflammatory bowel disease. Semin Thromb Hemost. 2013; 39 (5): 461-468.
6. Zitomersky NL, Verhave M, Trenor CC III,. Thrombosis and inflammatory bowel disease: a call for improved awareness and prevention. Inflamm Bowel Dis. 2011; 17 (1): 458-470.
7. Talbot RW, Heppell J, Dozois RR, Beart RW Jr,. Vascular complications of inflammatory bowel disease. Mayo Clin Proc. 1986; 61 (2): 140-145.
8. Webberley MJ, Hart MT, Melikian V,. Thromboembolism in inflammatory bowel disease: role of platelets. Gut. 1993; 34 (2): 247-251.
9. Sloan WP Jr, Bargen JA, Gage RB,. Life histories of patients with chronic ulcerative colitis: a review of 2000 cases. Gastroenterology. 1968; 54 (4 suppl): 819-822.
10. Bernstein CN, Blanchard JF, Rawsthorne P, Yu N,. The prevalence of extraintestinal diseases in inflammatory bowel disease: a population based study. Am J Gastroenterol. 2001; 96 (4): 1116-1122.
11. Peyrin-Biroulet L, Loftus EV Jr, Colombel JF, Sandborn WJ,. Long-term complications, extraintestinal manifestations, and mortality in adult Crohn's disease in population-based cohorts. Inflamm Bowel Dis. 2011; 17 (1): 471-478.
12. 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 (3): 430-444.
13. Huerta C, Johansson S, Wallander MA, García Rodríguez LA,. Risk factors and short-term mortality of venous thromboembolism diagnosed in the primary care setting in the United Kingdom. Arch Inten Med. 2007; 167 (9): 935-943.
14. Grainge MJ, West J, Card TR,. Venous thromboembolism during active disease and remission in inflammatory bowel disease: a cohort study. Lancet. 2010; 375 (9715): 657-663.
15. Kappelman MD, Horvath-Puho E, Sandler RS, et al. Thromboembolic risk among Danish children and adults with inflammatory bowel diseases: a population-based nationwide study. Gut. 2011; 60 (7): 937-943.
16. Nguyen GC, Sam J,. Rising prevalence of venous thromboembolism and its impact on mortality among hospitalized inflammatory bowel disease patients. Am J Gastroenterol. 2008; 103 (9): 2272-2280.
17. Novacek G, Weltermann A, Sobala A, et al. Inflammatory bowel disease is a risk factor for recurrent venous thromboembolism. Gastroenterology. 2010; 139 (3): 779-787.
18. Ha C, Magowan S, Accortt NA, Chen J, Stone CD,. Risk of arterial thrombotic events in inflammatory bowel disease. Am J Gastroenterol. 2009; 104 (6): 1445-1451.
19. Singh S, Singh H, Loftue EV Jr, Pardi DS,. Risk of cerebrovascular accidents and ischemic heart disease in patients with inflammatory bowel disease: a systematic review and meta-analysis. Clin Gastroenterol Hepatol. 2014; 12 (3): 382-393.
20. Bernstein CN, Wajda A, Blanchard JF,. The incidence of arterial thromboembolic diseases in inflammatory bowel disease: a population-based study. Clin Gastroenterol Hepatol. 2008; 6 (1): 41-45.
21. Yuhara H, Steinmaus C, Corley D, et al. Meta-analysis: the risk of venous thromboembolism in patients with inflammatory bowel disease. Aliment Pharmacol Ther. 2013; 37 (10): 953-962.
22. Miehsler W, Reinisch W, Valic E, et al. Is inflammatory bowel disease an independent and disease specific risk factor for thromboembolism? Gut. 2004; 53 (4): 542-548.
23. Thompson NP, Wakefield AJ, Pounder RE,. Inherited disorders of coagulation appear to protect against inflammatory bowel disease. Gastroenterology. 1995; 108 (4): 1011-1015.
24. Wakefield AJ, Sawyerr AM, Dhillon AP, et al. Pathogenesis of Crohn's disease: multifocal gastrointestinal infarction. Lancet. 1989; 2 (8571): 1057-1062.
25. Lazzerini M, Bramuzzo M, Maschio M, Martelossi S, Ventura A,. Thromboembolism in pediatric inflammatory bowel disease: systematic review. Inflamm Bowel Dis. 2011; 17 (10): 2174-2183.
26. Bertina RM, Koeleman BP, Koster T, et al. Mutation in blood coagulation factor V associated with resistance to activated protein C. Nature. 1994; 369 (6475): 64-67.
27. Seligsohn U, Lubetsky A,. Genetic susceptibility to venous thrombosis. N Engl J Med. 2001; 344 (16): 1222-1231.
28. Rees DC, Cox M, Clegg JB,. Word distribution of factor V Leiden. Lancet. 1995; 346 (8893): 1133-1134.
29. Papa A, Danese S, Grillo A, Gasbarrini G, Gasbarrini A,. Review article: inherited thrombophilia in inflammatory bowel disease. Am J Gastroenterol. 2003; 98 (6): 1247-1251.
30. Tsiolakidou G, Koutroubakis IE,. Thrombosis and inflammatory bowel disease-the role of genetic risk factors. World J Gastroenterol. 2008; 14 (28): 4440-4444.
31. Zhong M, Dong XW, Zheng Q, Tong JL, Ran ZH,. Factor V Leiden and thrombosis in patients with inflammatory bowel disease (IBD): a meta-analysis. Thromb Res. 2011; 128 (5): 403-409.
32. Cakal B, Gokmen A, Yalinkilic M, et al. Natural anticoagulant protein levels in Turkish patients with inflammatory bowel disease. Blood Coagul Fibrinolysis. 2010; 21 (2): 118-121.
33. Alkim H, Ayaz S, Alkim C, et al. Protein C pathway and antithrombin in thrombosis related gastrointestinal disorders. Turk J Acad Gastroenterol. 2010; 9 (2): 48-54.
34. Papa A, De Stefano V, Danese S, et al. Hyperhomocysteinemia and prevalence of polymorphisms of homocysteine metabolism-related enzymes in patients with inflammatory bowel disease. Am J Gastroenterol. 2001; 96 (9): 2677-2682.
35. Saibeni S, Cattaneo M, Vecchi M, et al. Low vitamin B(6) levels, a risk factor for thrombosis, in inflammatory bowel disease: role of inflammation and correlation with acute phase reactants. Am J Gastroenterol. 2003; 98 (1): 112-117.
36. Danese S, Papa A,. PAI-1 and TAFI in inflammatory bowel disease: the yin and yang of the fibrinolytic system. Eur J Gastroenterol Hepatol. 2008; 20 (9): 826-828.
37. Karimi O, Crusius JB, Coucoutsi C, et al. JAK2 V617F mutation is not involved in thromboembolism in IBD. Inflamm Bowel Dis. 2008; 14 (11): 1606-1607.
38. Gusella JF, Podolsky DK,. Inflammatory bowel disease: is it in the genes? Gastroenterology. 1998; 115 (5): 1286-1289.
39. Vecchi M, Sacchi E, Saibeni S, et al. Inflammatory bowel diseases are not associated with major hereditary conditions predisposing to thrombosis. Dig Dis Sci. 2000; 45 (7): 1465-1469.
40. Kjeldsen J, Lassen JF, Brandslund I, Schaffalitzky de Muckadell OB,. Markers of coagulation and fibrinolysis as measures of disease activity in inflammatory bowel disease. Scand J Gastroenterol. 1998; 33 (6): 637-643.
41. Hippisley-Cox J, Coupland C,. Development and validation of risk prediction algorithm (Q Thrombosis) to estimate future risk of venous thromboembolism: prospective cohort study. BMJ. 2011; 343: d4656.
42. van Dullemen H, Meenan J, Stronkhorst A, Tytgat GN, van Deventer SJ,. Mediators of mucosal inflammation: implications for therapy. Scand J Gastroenterol. 1997; 223: 92-98.
43. Wardle TD, Hall L, Turnberg LA,. Platelet activating factor: release from colonic mucosa in patients with ulcerative colitis and its effect on colonic secretion. Gut. 1996; 38 (3): 355-361.
44. Esmon CT,. The interactions between inflammation and coagulation. Br J Haematol. 2005; 131 (4): 417-430.
45. Alkim H, Ayaz S, Alkim C, Ulker A, Sahin B,. Continuous active state of coagulation system in patients with nonthrombotic inflammatory bowel disease. Clin Appl Thromb Hemost. 2011; 17 (6): 600-604.
46. Saibeni S, Saladino V, Chantarangkul V, et al. Increased thrombin generation in inflammatory bowel diseases. Thromb Res. 2010; 125 (3): 278-282.
47. El Accaoui RN, Shamseddeen WA, Taher AT,. Thalidomide and thrombosis. A meta-analysis. Thromb Haemost. 2007; 97 (6): 1031-1036.
48. Vazquez SR, Rondina MT, Pendleton RC,. Azathioprine-induced warfarin resistance. Ann Pharmacother. 2008; 42 (7): 1118-1123.
49. Peyrin-Biroulet L, Rodriguez-Gueant RM, Chamaillard M, et al. Vascular and cellular stress in inflammatory bowel disease: revisiting the role of homocysteine. Am J Gasstroenterol. 2007; 102 (5): 1108-1115.
50. Murata S, Ishikawa N, Oshikawa S, et al. Cerebral sinus thrombosis associated with severe ulcerative colitis. Intern Med. 2004; 43 (5): 400-403.
51. Margreiter R, European Tacrolimus vs Ciclosporin Microemulsion Renal Transplantation Study Group. Efficacy and safety of tacrolimus compared with cyclosporine microemulsion in renal transplantation: a randomised multicentre study. Lancet. 2002; 359 (9308): 741-746.
52. Danese S, Sans M, Scaldaferri F, et al. TNF-alpha blockade downregulates the CD40/CD40 L pathway in the mucosal microcirculation: a novel anti-inflammatory mechanism of infliximab in Crohn's disease. J Immunol. 2006; 176 (4): 2617-2624.
53. Reddy JG, Loftus EV Jr,. Safety of infliximab and other biologic agents in the inflammatory bowel diseases. Gastroenterol Clin North Am. 2006; 35 (4): 837-855.
54. Papa A, Danese S, Gasbarrini A, et al. Review article: potential therapeutic applications and mechanisms of action of heparin in inflammatory bowel disease. Aliment Pharmacol Ther. 2000; 14 (11): 1403-1409.
55. Young E,. The anti-inflammatory effects of heparin and related compounds. Thromb Res. 2008; 122 (6): 743-752.
56. Gaffney PR, Doyle CT, Gaffney A, Hogan J, Hayes DP, Annis P,. Paradoxical response to heparin in 10 patients with ulcerative colitis. Am J Gastroenterol. 1995; 90 (2): 220-223.
57. Evans RC, Wong VS, Morris AI, Rhodes JM,. Treatment of corticosteroid resistant ulcerative colitis with heparin-a report of 16 cases. Aliment Pharmacol Ther. 1997; 11 (6): 1037-1040.
58. Folwaczny C, Wiebecke B, Loeschke K,. Unfractioned heparin in the therapy of patients with highly active inflammatory bowel disease. Am J Gastroenterol. 1999; 94 (6): 1551-1555.
59. Törkvist L, Thorlacius H, Sjöqvist U, et al. Low molecular weight heparin as adjuvant therapy in active ulcerative colitis. Aliment Pharmacol Ther. 1999; 13 (10): 1323-1328.
60. Shen J, Ran ZH, Tong JL, Xiao SD,. Meta-analysis: the utility and safety of heparin in the treatment of active ulcerative colitis. Aliment Phermacol Ther. 2007; 26 (5): 653-663.
61. Sorensen GV, Erichsen R, Svaerke C, Farkas DK, Sørensen HT,. Risk of cancer in patients with inflammatory bowel disease and venous thromboembolism: a nationwide cohort study. Inflamm Bowel Dis. 2012; 18 (10): 1959-1963.
62. Kornbluth A, Sachar DB, Practice Parameters Committee of the American College of Gastroenterology. Ulcerative colitis practice guidelines in adults: American College of Gastroenterology, Practice Parameters Committee. Am J Gastroenterol. 2010; 105 (3): 501-523.
63. Guyatt GH, Norris SL, Schulman S, et al. Methodology for the development of antithrombotic therapy and prevention of thrombosis guidelines: Antithrombotic therapy and prevention of thrombosis, 9th ed: American College of Chest Physicians Evidence-Based Clinical Practice Guidelines. Chest. 2012; 141 (2 suppl): 53S-70S.
64. Mowat C, Cole A, Windsor A, et al. Guidelines for the management of inflammatory bowel disease in adults. Gut. 2011; 60 (5): 571-607.
65. Van Assche G, Dignass A, Bokemeyer B, et al. Second European evidence-based consensus on the management of ulcerative colitis part 3: special situations. J Crohns Colitis. 2013; 7 (1): 1-33.
66. Van Assche G, Dignass A, Reinisch W, et al. The second European evidence-based consensus on the management of Crohn's disease: special situations. J Crohns Colitis. 2010; 4 (1): 63-101.
67. Aryal KR, Al-Khaffaf H,. Venous thromboembolic complications following air travel: what's the quantitative risk? A literature review. Eur J Vasc Endovasc Surg. 2006; 31 (2): 187-199.
68. Tinsley A, Naymagon S, Trindade AJ, Sachar DB, Sands BE, Ullman TA,. A survey of current practice of venous thromboembolism prophylaxis in hospitalized inflammatory bowel disease patients in the United States. J Clin Gastroenterol. 2013; 47 (1): e1-e6.
69. Ananthakrishnan AN, Higuchi LM, Huang ES, et al. Aspirin, nonsteroidal anti-inflammatory drug use, and risk for Crohn disease and ulcerative colitis: a cohort study. Ann Intern Med. 2012; 156 (5): 350-359.
70. Kefalakes H, Stylianides TJ, Amanakis G, Kolios G,. Exacerbation of inflammatory bowel diseases associated with the use of nonsteroidal anti- inflammatory drugs: myth or reality? Eur J Clin Pharmacol. 2009; 65 (10): 963-970.
71. Bryant RV, Jairath V, Curry N, Travis SP,. Thrombosis in inflammatory bowel disease: are we tailoring prophylaxis to those most at risk? J Crohns Colitis. 2014; 8 (2): 166-171.
72. Nguyen GC, Sharma S,. Feasibility of venous thromboembolism prophylaxis during inflammatory bowel disease flares in the outpatient setting: a decision analysis. Inflamm Bowel Dis. 2013; 19 (10): 2182.
73. Nguyen GC, Bernstein CN,. Duration of anticoagulation for the management of venous thromboembolism in inflammatory bowel disease: a decision analysis. Am J Gastroenterol. 2013; 108 (9): 1486.
74. Gross ME, Vogler SA, Mone MC, Sheng X, Sklow B,. The importance of extended postoperative venous thromboembolism prophylaxis in IBD. A national surgical quality improvement program analysis. Dis Colon Rectum. 2014; 57 (4): 482-489.
75. Nguyen GC, Bernstein CN, Bitton A, et al. Consensus statements on the risk, prevention, and treatment of venous thromboembolism in inflammatory bowel disease: Canadian Association of Gastroenterology. Gastroenterology. 2014; 146 (3): 835-848.