Association of Venous Thromboembolism and Inflammatory Bowel Disease

Document Type : Review Article

Authors

1 Department of Gastroenterology and Hepatology, Mashhad University of Medical Sciences, Mashhad, Iran.

2 Student Research Committee, Islamic Azad University, Mashhad Branch, Mashhad, Iran.

3 Department of Internal Medicine, Faculty of Medicine, Mashhad University of Medical Sciences, Mashhad, Iran.

4 Department of Internal Medicine, University of Toronto, Toronto, Canada.

Abstract

Introduction: Studies have shown that patients with inflammatory bowel disease (IBD) have an increased risk for venous thromboembolism (VTE). VTEs causes significant morbidity and mortality.
Methods: We carried out a comprehensive search through different online databases including PubMed, Google Scholar, Scopus, and Medline. We focused on some of patients-related factors that may affect the risk of VTE incidence among IBD patients and also reviewed current guidelines on the prophylactic regimen of the IBD patients.
Results: Based on the previous studies, the hypercoagulable nature of the disease results from a complex interaction between the systems participating in the coagulation cascade, including endothelial cells, platelets, and coagulation factors. There are a number of clinical factors that increase the probability of VTE development which include disease activity, age, pregnancy, surgery, and medical treatment.
Conclusion: Taken together, these data suggest to initiate prophylactic regimen in IBD patients and to adjust it regarding to the patient’s condition and the presence of other predisposing factors.

Keywords


  1. Baumgart DC, Carding SR. Inflammatory bowel disease: cause and immunobiology. The Lancet. 2007 May 12;369(9573):1627-40
  2. Kaplan GG. The global burden of IBD: from 2015 to 2025. Nature reviews Gastroenterology & hepatology. 2015 Dec;12(12):720-7.
  3. Burisch J, Jess T, Martinato M, Lakatos PL, ECCO-EpiCom. The burden of inflammatory bowel disease in Europe. Journal of Crohn's and Colitis. 2013 May 1;7(4):322-37.
  4. Murthy SK, Nguyen GC. Venous thromboembolism in inflammatory bowel disease: an epidemiological review. Official journal of the American College of Gastroenterology| ACG. 2011 Apr 1;106(4):713-8.
  5. Miehsler W, Reinisch W, Valic E, Osterode W, Tillinger W, Feichtenschlager T, et al. Is inflammatory bowel disease an independent and disease specific risk factor for thromboembolism? Gut. 2004;53(4):542-8.
  6. Solem CA, Loftus Jr EV, Tremaine WJ, Sandborn WJ. Venous thromboembolism in inflammatory bowel disease. Official journal of the American College of Gastroenterology| ACG. 2004 Jan 1;99(1):97-101.
  7. 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. Thrombosis and haemostasis. 2001;85(03):430-4.
  8. Nguyen GC, Sam J. Rising prevalence of venous thromboembolism and its impact on mortality among hospitalized inflammatory bowel disease patients. Official journal of the American College of Gastroenterology| ACG. 2008 Sep 1;103(9):2272-80.
  9. Kappelman MD, Horvath-Puho E, Sandler RS, Rubin DT, Ullman TA, Pedersen L, et al. Thromboembolic risk among Danish children and adults with inflammatory bowel diseases: a population-based nationwide study. Gut. 2011 Jul 1;60(7):937-43.
  10. Yuhara H, Steinmaus C, Corley D, Koike J, Igarashi M, Suzuki T, et al. Meta‐analysis: the risk of venous thromboembolism in patients with inflammatory bowel disease. Alimentary pharmacology & therapeutics. 2013 May;37(10):953-62.
  11. Papa A, Gerardi V, Marzo M, Felice C, Rapaccini GL, Gasbarrini A. Venous thromboembolism in patients with inflammatory bowel disease: focus on prevention and treatment. World Journal of Gastroenterology: WJG. 2014 Mar 3;20(12):3173.
  12. Grainge MJ, West J, Card TR. Venous thromboembolism during active disease and remission in inflammatory bowel disease: a cohort study. The Lancet. 2010 Feb 20;375(9715):657-63.
  13. Danese S, Papa A, Saibeni S, Repici A, Malesci A, Vecchi M. Inflammation and Coagulation in Inflammatory Bowel Disease: The Clot Thickens: CME. Official journal of the American College of Gastroenterology| ACG. 2007 Jan 1;102(1):174-86.
  14. Nguyen GC, Boudreau H, Harris ML, Maxwell CV. Outcomes of obstetric hospitalizations among women with inflammatory bowel disease in the United States. Clinical Gastroenterology and Hepatology. 2009 Mar 1;7(3):329-34.
  15. TALBOT RW, Heppell JA, DOZOIS RR, BEART Jr RW. Vascular complications of inflammatory bowel disease. InMayo Clinic Proceedings 1986 Feb 1 (Vol. 61, No. 2, pp. 140-145). Elsevier.
  16. Johns DR. Cerebrovascular complications of inflammatory bowel disease. American Journal of Gastroenterology (Springer Nature). 1991 Mar 1;86(3).
  17. Landman C, Nahon S, Cosnes J, Bouhnik Y, Brixi-Benmansour H, Bouguen G, et al. Portomesenteric vein thrombosis in patients with inflammatory bowel disease. Inflammatory Bowel Diseases. 2013 Mar 1;19(3):582-9.
  18. Schneiderman JH, Sharpe JA, Sutton DM. Cerebral and retinal vascular complications of inflammatory bowel disease. Annals of Neurology: Official Journal of the American Neurological Association and the Child Neurology Society. 1979 Apr;5(4):331-7.
  19. Hatoum OA, Spinelli KS, Abu-Hajir M, Attila T, Franco J, Otterson MF, et al. Mesenteric venous thrombosis in inflammatory bowel disease. Journal of clinical gastroenterology. 2005;39(1):27-31.
  20. Papay P, Miehsler W, Tilg H, Petritsch W, Reinisch W, Mayer A, et al. Clinical presentation of venous thromboembolism in inflammatory bowel disease. Journal of Crohn's and Colitis. 2013;7(9):723-9.
  21. Nylund CM, Goudie A, Garza JM, Crouch G, Denson LA. Venous thrombotic events in hospitalized children and adolescents with inflammatory bowel disease. Journal of pediatric gastroenterology and nutrition. 2013;56(5):485-91.
  22. Nguyen GC, Bernstein CN, Bitton A, Chan AK, Griffiths AM, Leontiadis GI, 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):835-48. e6.
  23. Ando K, Fujiya M, Nomura Y, Inaba Y, Sugiyama Y, Kobayashi Y, et al. The incidence and risk factors of venous thromboembolism in patients  with  inflammatory   bowel  disease:   a  prospective multicenter cohort study. Digestion. 2019;100(4):229-37.
  24. Faye AS, Wen T, Ananthakrishnan AN, Lichtiger S, Kaplan GG, Friedman AM, et al. Acute venous thromboembolism risk highest within 60 days after discharge from the hospital in patients with inflammatory bowel diseases. Clinical Gastroenterology and Hepatology. 2020;18(5):1133-41. e3.
  25. McCurdy JD, Israel A, Hasan M, Weng R, Mallick R, Ramsay T, et al. A clinical predictive model for post‐hospitalisation venous thromboembolism in patients with inflammatory bowel disease. Alimentary Pharmacology & Therapeutics. 2019;49(12):1493-501.
  26. Jeuring SF, van den Heuvel TR, Zeegers MP, Hameeteman WH, Romberg-Camps MJ, Oostenbrug LE, et al. Epidemiology and long-term outcome of inflammatory bowel disease diagnosed at elderly age—an increasing distinct entity? Inflammatory bowel diseases. 2016;22(6):1425-34.
  27. Hansen A, Erichsen R, Horváth‐Puhó E, Sørensen H. Inflammatory bowel disease and venous thromboembolism during pregnancy and the postpartum period. Journal of Thrombosis and Haemostasis. 2017;15(4):702-8.
  28. Bollen L, Casteele NV, Ballet V, Van Assche G, Ferrante M, Vermeire S, et al. Thromboembolism as an important complication of inflammatory bowel disease. European journal of gastroenterology & hepatology. 2016;28(1):1-7.
  29. Weng M-T, Park SH, Matsuoka K, Tung C-C, Lee JY, Chang C-H, et al. Incidence and risk factor analysis of thromboembolic events in East Asian patients with inflammatory bowel disease, a multinational collaborative study. Inflammatory bowel diseases. 2018;24(8):1791-800.
  30. Kim YH, Pfaller B, Marson A, Yim HW, Huang V, Ito S. The risk of venous thromboembolism in women with inflammatory bowel disease during pregnancy and the postpartum period: a systematic review and meta-analysis. Medicine. 2019;98(38).
  31. Jackson E, Curtis KM, Gaffield ME. Risk of venous thromboembolism during the postpartum period: a systematic review. Obstetrics & Gynecology. 2011;117(3):691-703.
  32. Kim SC, Schneeweiss S, Liu J, Solomon DH. Risk of venous thromboembolism in patients with rheumatoid arthritis. Arthritis care & research. 2013;65(10):1600-7.
  33. Carty E, MacEy M, Rampton D. Inhibition of platelet activation by 5-aminosalicylic acid in inflammatory bowel disease. Alimentary pharmacology & therapeutics. 2000;14(9):1169-79.
  34. Thomas G, Skrinska VA, Lucas FV. The influence of glutathione and other thiols on human platelet aggregation. Thrombosis research. 1986;44(6):859-66.
  35. Sarlos P, Szemes K, Hegyi P, Garami A, Szabo I, Illes A, et al. Steroid but not biological therapy elevates the risk of venous thromboembolic events in inflammatory bowel disease: a meta-analysis. Journal of Crohn's and Colitis. 2018;12(4):489-98.
  36. Johannesdottir SA, Horváth-Puhó E, Dekkers OM, Cannegieter SC, Jørgensen JOL, Ehrenstein V, et al. Use of glucocorticoids and risk of venous thromboembolism: a nationwide population-based case-control study. JAMA internal medicine. 2013;173(9):743-52.
  37. van der Pas R, Leebeek F, Hofland L, De Herder W, Feelders R. Hypercoagulability in C ushing's syndrome: prevalence, pathogenesis and treatment. Clinical endocrinology. 2013;78(4):481-8.
  38. Ananthakrishnan AN, Cagan A, Gainer VS, Cheng S-C, Cai T, Scoville E, et al. Thromboprophylaxis is associated with reduced post-hospitalization venous thromboembolic events in patients with inflammatory bowel diseases. Clinical Gastroenterology and Hepatology. 2014;12(11):1905-10.
  39. Yoshida H, Yilmaz CE, Granger ND. Role of tumor necrosis factor-α in the extraintestinal thrombosis associated with colonic inflammation. Inflammatory Bowel Diseases. 2011;17(11):2217-23.
  40. DeFonseka AM, Tuskey A, Conaway MR, Behm BW. Antitumor necrosis factor-α therapy is associated with reduced risk of thromboembolic events in hospitalized patients with inflammatory bowel disease. Journal of clinical gastroenterology. 2016;50(7):578-83.
  41. Higgins PD, Skup M, Mulani PM, Lin J, Chao J. Increased risk of venous thromboembolic events with corticosteroid vs biologic therapy for inflammatory bowel disease. Clinical Gastroenterology and Hepatology. 2015;13(2):316-21.
  42. Sandborn WJ, Panés J, Sands BE, Reinisch W, Su C, Lawendy N, et al. Venous thromboembolic events in the tofacitinib ulcerative colitis clinical development programme. Alimentary Pharmacology & Therapeutics. 2019;50(10):1068-76.
  43. Heit JA. Venous thromboembolism: disease burden, outcomes and risk factors. Journal of Thrombosis and Haemostasis. 2005;3(8):1611-7.
  44. Fleming F, Gaertner W, Ternent CA, Finlayson E, Herzig D, Paquette IM, et al. The American Society of Colon and Rectal Surgeons clinical practice guideline for the prevention of venous thromboembolic disease in colorectal surgery. Diseases of the Colon & Rectum. 2018;61(1):14-20.
  45. McLeod RS, Geerts WH, Sniderman KW, Greenwood C, Gregoire RC, Taylor BM, et al. Subcutaneous heparin versus low-molecular-weight heparin as thromboprophylaxis in patients undergoing colorectal surgery: results of the canadian colorectal DVT prophylaxis trial: a randomized, double-blind trial. Annals of surgery. 2001;233(3):438.
  46. Alhassan N, Trepanier M, Sabapathy C, Chaudhury P, Liberman A, Charlebois P, et al. Risk factors for post-discharge venous thromboembolism in patients undergoing colorectal resection: a NSQIP analysis. Techniques in coloproctology. 2018;22:955-64.
  47. Alatri A, Schoepfer A, Fournier N, Engelberger RP, Safroneeva E, Vavricka S, et al. Prevalence and risk factors for venous thromboembolic complications in the Swiss Inflammatory Bowel Disease Cohort. Scandinavian journal of gastroenterology. 2016;51(10):1200-5.
  48. Kakkar V, Balibrea J, Martinez‐Gonzalez J, Prandoni P, Group CS. Extended prophylaxis with bemiparin for the prevention of venous thromboembolism after abdominal or pelvic surgery for cancer: the CANBESURE randomized study. Journal of Thrombosis and Haemostasis. 2010;8(6):1223-9.
  49. Bergqvist D, Agnelli G, Cohen AT, Eldor A, Nilsson PE, Le Moigne-Amrani A, et al. Duration of prophylaxis against venous thromboembolism with enoxaparin after surgery for cancer. New England Journal of Medicine. 2002;346(13):975-80.
  50. Rasmussen MS, Jørgensen LN, Wille‐Jørgensen P. Prolonged thromboprophylaxis with low molecular weight heparin for abdominal or pelvic surgery. Cochrane database of systematic reviews. 2009(1).
  51. Gould MK, Garcia DA, Wren SM, Karanicolas PJ, Arcelus JI, Heit JA, et al. Prevention of VTE in nonorthopedic surgical patients: antithrombotic therapy and prevention of thrombosis: American College of Chest Physicians Evidence-Based Clinical Practice Guidelines. Chest. 2012;141(2):e227S-e77S.
  52. Oldenburg B, Van Tuyl BA, van der Griend R, Fijnheer R, van Berge Henegouwen GP. Risk factors for thromboembolic complications in inflammatory bowel disease: the role of hyperhomocysteinaemia. Digestive diseases and sciences. 2005;50:235-40.
  53. Kahn SR, Lim W, Dunn AS, Cushman M, Dentali F, Akl EA, et al. Prevention of VTE in nonsurgical patients: antithrombotic therapy and prevention of thrombosis: American College of Chest Physicians Evidence-Based Clinical Practice Guidelines. Chest. 2012;141(2):e195S-e226S.
  54. Van Assche G, Dignass A, Panes J, Beaugerie L, Karagiannis J, Allez M, et al. The second European evidence-based consensus on the diagnosis and management of Crohn's disease: definitions and diagnosis. Journal of Crohn's and Colitis. 2010;4(1):7-27.
  55. Mowat C, Cole A, Windsor A, Ahmad T, Arnott I, Driscoll R, et al. Guidelines for the management of inflammatory bowel disease in adults. Gut. 2011;60(5):571-607.
  56. Kornbluth A, Sachar D. Ulcerative colitis practice guidelines in adults. American College of Gastroenterology, Practice Parameters Committee. The American journal of gastroenterology. 1997;92(2):204-11.
  57. Dentali F, Douketis JD, Gianni M, Lim W, Crowther MA. Meta-analysis: anticoagulant prophylaxis to prevent symptomatic venous thromboembolism in hospitalized medical patients. Annals of internal medicine. 2007;146(4):278-88.
  58. Leizorovicz A, Cohen AT, Turpie AG, Olsson C-G, Vaitkus PT, Goldhaber SZ. Randomized, placebo-controlled trial of dalteparin for the prevention of venous thromboembolism in acutely ill medical patients. Circulation. 2004;110(7):874-9.
  59. Scarpa M, Pilon F, Pengo V, Romanato G, Ruffolo C, Erroi F, et al. Deep venous thrombosis after surgery for inflammatory bowel disease: is standard dose low molecular weight heparin prophylaxis enough? World journal of surgery. 2010;34:1629-36.
  60. O’Connor OJ, Cahill RA, Kirwan WO, Redmond HP. The incidence of postoperative venous thrombosis among patients with ulcerative colitis. Irish journal of medical science. 2005;174:20-2.
  61. Novacek G, Weltermann A, Sobala A, Tilg H, Petritsch W, Reinisch W, et al. Inflammatory bowel disease is a risk factor for recurrent venous thromboembolism. Gastroenterology. 2010;139(3):779-87. e1.
  62. Nguyen GC, Bernstein CN. Duration of anticoagulation for the management of venous thromboembolism in inflammatory bowel disease: a decision analysis. Official journal of the American College of Gastroenterology| ACG. 2013;108(9):1486-95.
  63. Tabibian JH, Streiff MB. Inflammatory bowel disease-associated thromboembolism: a systematic review of outcomes with anticoagulation versus catheter-directed thrombolysis. Inflammatory bowel diseases. 2012;18(1):161-71.
  64. Lopez PR, Stewart DW, Smalligan RD. Recurrent deep vein thrombosis despite warfarin therapy in a patient with Crohn's disease. Postgraduate Medicine. 2010;122(3):181-4.
  65. Huerta C, Johansson S, Wallander M-A, Rodríguez LAG. Risk factors and short-term mortality of venous thromboembolism diagnosed in the primary care setting in the United Kingdom. Archives of internal medicine. 2007;167(9):935-43.