General Review Article

Thrombosis in IBD in the Era of JAK Inhibition

Author(s): Virginia Solitano, Gionata Fiorino, Ferdinando D’Amico, Laurent Peyrin-Biroulet and Silvio Danese*

Volume 22, Issue 1, 2021

Published on: 02 September, 2020

Page: [126 - 136] Pages: 11

DOI: 10.2174/1389450121666200902164240

Price: $65

Abstract

Patients with inflammatory bowel diseases (IBD) have an increased risk of thrombosis. The interaction between inflammation and coagulation has extensively been studied. It is well-- known that some drugs can influence the haemostatic system, but several concerns on the association between therapies and increased risk of thrombosis remain open. While biologics seem to have a protective role against thrombosis via their anti-inflammatory effect, some concerns about an increased risk of thrombosis with JAK inhibitors have been raised. We conducted a literature review to assess the association between biologics/small molecules and venous/arterial thrombotic complications. An increased risk of venous and arterial thrombosis was found in patients treated with corticosteroids, whereas anti-TNFα were considered protective agents. No thromboembolic adverse event was reported with vedolizumab and ustekinumab. In addition, thromboembolic events rarely occurred in patients with ulcerative colitis (UC) after therapy with tofacitinib. The overall risk of both venous and arterial thrombosis was not increased based on the available evidence. Finally, in the era of JAK inhibitors, the treatment should be individualized by evaluating the pre-existing potential thrombotic risk balanced with the intrinsic risk of the medication used.

Keywords: Inflammatory bowel disease, thrombosis, corticosteroids, anti-TNFα, vedolizumab, ustekinumab, JAK inhibitors

Graphical Abstract
[1]
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): 2272-80.
[http://dx.doi.org/10.1111/j.1572-0241.2008.02052.x] [PMID: 18684186]
[2]
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): 430-4.
[http://dx.doi.org/10.1055/s-0037-1615600] [PMID: 11307809]
[3]
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): 937-43.
[http://dx.doi.org/10.1136/gut.2010.228585] [PMID: 21339206]
[4]
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): 953-62.
[http://dx.doi.org/10.1111/apt.12294] [PMID: 23550660]
[5]
Saleh T, Matta F, Yaekoub AY, Danescu S, Stein PD. Risk of venous thromboembolism with inflammatory bowel disease. Clin Appl Thromb Hemost 2011; 17(3): 254-8.
[http://dx.doi.org/10.1177/1076029609360528] [PMID: 20211927]
[6]
Fumery M, Xiaocang C, Dauchet L, Gower-Rousseau C, Peyrin-Biroulet L, Colombel JF. Thromboembolic events and cardiovascular mortality in inflammatory bowel diseases: a meta-analysis of observational studies. J Crohn’s Colitis 2014; 8(6): 469-79.
[http://dx.doi.org/10.1016/j.crohns.2013.09.021] [PMID: 24183231]
[7]
Danese S, Papa A, Saibeni S, Repici A, Malesci A, Vecchi M. Inflammation and coagulation in inflammatory bowel disease: The clot thickens. Am J Gastroenterol 2007; 102(1): 174-86.
[http://dx.doi.org/10.1111/j.1572-0241.2006.00943.x] [PMID: 17100967]
[8]
Papa A, Danese S, Grillo A, Gasbarrini G, Gasbarrini A. Review article: inherited thrombophilia in inflammatory bowel disease. Am J Gastroenterol 2003; 98(6): 1247-51.
[http://dx.doi.org/10.1111/j.1572-0241.2003.07491.x] [PMID: 12818264]
[9]
Bayan K, Tüzün Y, Yilmaz S, Canoruc N, Dursun M. Analysis of inherited thrombophilic mutations and natural anticoagulant deficiency in patients with idiopathic portal hypertension. J Thromb Thrombolysis 2009; 28(1): 57-62.
[http://dx.doi.org/10.1007/s11239-008-0244-8] [PMID: 18685811]
[10]
Magro F, Soares JB, Fernandes D. Venous thrombosis and prothrombotic factors in inflammatory bowel disease. World J Gastroenterol 2014; 20(17): 4857-72.
[http://dx.doi.org/10.3748/wjg.v20.i17.4857] [PMID: 24803797]
[11]
Grainge MJ, West J, Card TR. Venous thromboembolism during active disease and remission in inflammatory bowel disease: a cohort study. Lancet 2010; 375(9715): 657-63.
[http://dx.doi.org/10.1016/S0140-6736(09)61963-2] [PMID: 20149425]
[12]
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, 787.e1.
[http://dx.doi.org/10.1053/j.gastro.2010.05.026] [PMID: 20546736]
[13]
Kristensen SL, Ahlehoff O, Lindhardsen J, et al. Disease activity in inflammatory bowel disease is associated with increased risk of myocardial infarction, stroke and cardiovascular death--a Danish nationwide cohort study. PLoS One 2013; 8(2): e56944.
[http://dx.doi.org/10.1371/journal.pone.0056944] [PMID: 23457642]
[14]
Oussalah A, Guéant JL, Peyrin-Biroulet L. Meta-analysis: hyperhomocysteinaemia in inflammatory bowel diseases. Aliment Pharmacol Ther 2011; 34(10): 1173-84.
[http://dx.doi.org/10.1111/j.1365-2036.2011.04864.x] [PMID: 21967576]
[15]
Tan VP, Chung A, Yan BP, Gibson PR. Venous and arterial disease in inflammatory bowel disease. J Gastroenterol Hepatol 2013; 28(7): 1095-113.
[http://dx.doi.org/10.1111/jgh.12260] [PMID: 23662785]
[16]
Kirchgesner J, Beaugerie L, Carrat F, Andersen NN, Jess T, Schwarzinger M. BERENICE study group. Increased risk of acute arterial events in young patients and severely active IBD: a nationwide French cohort study. Gut 2018; 67(7): 1261-8.
[http://dx.doi.org/10.1136/gutjnl-2017-314015] [PMID: 28647686]
[17]
Higgins PDR, Skup M, Mulani PM, Lin J, Chao J. Increased risk of venous thromboembolic events with corticosteroid vs biologic therapy for inflammatory bowel disease. Clin Gastroenterol Hepatol 2015; 13(2): 316-21.
[http://dx.doi.org/10.1016/j.cgh.2014.07.017] [PMID: 25038374]
[18]
Johannesdottir SA, Horváth-Puhó E, Dekkers OM, et al. Use of glucocorticoids and risk of venous thromboembolism: a nationwide population-based case-control study. JAMA Intern Med 2013; 173(9): 743-52.
[http://dx.doi.org/10.1001/jamainternmed.2013.122] [PMID: 23546607]
[19]
Rungoe C, Basit S, Ranthe MF, Wohlfahrt J, Langholz E, Jess T. Risk of ischaemic heart disease in patients with inflammatory bowel disease: a nationwide Danish cohort study. Gut 2013; 62(5): 689-94.
[http://dx.doi.org/10.1136/gutjnl-2012-303285] [PMID: 22961677]
[20]
FDA approves Boxed Warning about increased risk of blood clots and death with higher dose of arthritis and ulcerative colitis medicine tofacitinib (Xeljanz, Xeljanz XR) | FDA https://www.fda.gov/drugs/drug-safety-and-availability/fda-approves-boxed-warning-about-increased-risk-blood-clots-and-death-higher-dose-arthritis-and
[21]
Olivera P, Danese S, Peyrin-Biroulet L. JAK inhibition in inflammatory bowel disease. Expert Rev Clin Immunol 2017; 13(7): 693-703.
[http://dx.doi.org/10.1080/1744666X.2017.1291342] [PMID: 28164724]
[22]
Sandborn WJ, Su C, Sands BE, et al. OCTAVE Induction 1, OCTAVE Induction 2, and OCTAVE Sustain Investigators. Tofacitinib as induction and maintenance therapy for ulcerative colitis. N Engl J Med 2017; 376(18): 1723-36.
[http://dx.doi.org/10.1056/NEJMoa1606910] [PMID: 28467869]
[23]
EMA confirms Xeljanz to be used with caution in patients at high risk of blood clots | European Medicines Agency https://www.ema.europa.eu/en/news/ema-confirms-xeljanz-be-used-caution-patients-high-risk-blood-clots
[24]
Safety Study Of Tofacitinib Versus Tumor Necrosis Factor (TNF) Inhibitor In Subjects With Rheumatoid Arthritis - Full Text View - ClinicalTrials https://clinicaltrials.gov/ct2/show/NCT02092467?term=A3921133&draw=2&rank=1
[25]
Alkim H, Koksal AR, Boga S, Sen I, Alkim C. Etiopathogenesis, Prevention, and Treatment of Thromboembolism in Inflammatory Bowel Disease. Clin Appl Thromb Hemost 2017; 23(6): 501-10.
[http://dx.doi.org/10.1177/1076029616632906] [PMID: 26893444]
[26]
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): 600-4.
[http://dx.doi.org/10.1177/1076029611405034] [PMID: 21593018]
[27]
Lagrange J, Lacolley P, Wahl D, Peyrin-Biroulet L, Regnault V. Shedding Light on Hemostasis in Patients With Inflammatory Bowel Diseases. Clin Gastroenterol Hepatol 2020.
[http://dx.doi.org/10.1016/j.cgh.2019.12.043] [PMID: 31972287]
[28]
Neurath MF. Current and emerging therapeutic targets for IBD. Nat Rev Gastroenterol Hepatol 2017; 14(5): 269-78.
[http://dx.doi.org/10.1038/nrgastro.2016.208] [PMID: 28144028]
[29]
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): 458-70.
[http://dx.doi.org/10.1002/ibd.21334] [PMID: 20848518]
[30]
van Zaane B, Nur E, Squizzato A, et al. Systematic review on the effect of glucocorticoid use on procoagulant, anti-coagulant and fibrinolytic factors. J Thromb Haemost 2010; 8(11): 2483-93.
[http://dx.doi.org/10.1111/j.1538-7836.2010.04034.x] [PMID: 20735729]
[31]
Yoshida H, Russell J, Granger DN. Pro-inflammatory cytokines mediate the extra-intestinal thrombus formation associated with inflammatory bowel disease (IBD). FASEB J 2009; 23.http://ovidsp.ovid.com/ovidweb.cgi?T=JS&PAGE=reference&D=emed12&NEWS=N&AN=70053652
[32]
Nawroth PP, Stern DM. Modulation of endothelial cell hemostatic properties by tumor necrosis factor. J Exp Med 1986; 163(3): 740-5.
[http://dx.doi.org/10.1084/jem.163.3.740] [PMID: 3753996]
[33]
Yoshida H, Yilmaz CE, Granger DN. Role of tumor necrosis factor-α in the extraintestinal thrombosis associated with colonic inflammation. Inflamm Bowel Dis 2011; 17(11): 2217-23.
[http://dx.doi.org/10.1002/ibd.21593] [PMID: 21987296]
[34]
Danese S, Sans M, Scaldaferri F, et al. TNF-α blockade down-regulates the CD40/CD40L pathway in the mucosal microcirculation: a novel anti-inflammatory mechanism of infliximab in Crohn’s disease. J Immunol 2006; 176(4): 2617-24.
[http://dx.doi.org/10.4049/jimmunol.176.4.2617] [PMID: 16456024]
[35]
Knapp S. New opportunities for kinase drug repurposing and target discovery. Br J Cancer 2018; 118(7): 936-7.
[http://dx.doi.org/10.1038/s41416-018-0045-6] [PMID: 29545596]
[36]
Hanke T, Wong JF, Berger BT, et al. A Highly Selective Chemical Probe for Activin Receptor-like Kinases ALK4 and ALK5. ACS Chem Biol 2020; 15(4): 862-70.
[http://dx.doi.org/10.1021/acschembio.0c00076] [PMID: 32176847]
[37]
Chaikuad A, Koschade SE, Stolz A, et al. Conservation of structure, function and inhibitor binding in UNC-51-like kinase 1 and 2 (ULK1/2). Biochem J 2019; 476(5): 875-87.
[http://dx.doi.org/10.1042/BCJ20190038] [PMID: 30782972]
[38]
Canduri F, Perez PC, Caceres RA, de Azevedo WF Jr. Protein kinases as targets for antiparasitic chemotherapy drugs. Curr Drug Targets 2007; 8(3): 389-98.
[http://dx.doi.org/10.2174/138945007780058979] [PMID: 17348832]
[39]
Filgueira de Azevedo W. Opinion Paper: Targeting Multiple Cyclin-Dependent Kinases (CDKs): A New Strategy for Molecular Docking Studies. Curr Drug Targets 2015; 17(1): 2.
[http://dx.doi.org/10.2174/138945011701151217100907] [PMID: 25330032]
[40]
Bitencourt-Ferreira G, Rizzotto C, de Azevedo Junior WF. Machine Learning-Based Scoring Functions. Development and Applications with SAnDReS. Curr Med Chem 2020; 27.
[PMID: 32410551]
[41]
Kiu H, Nicholson SE. Biology and significance of the JAK/STAT signalling pathways. Growth Factors 2012; 30(2): 88-106.
[http://dx.doi.org/10.3109/08977194.2012.660936] [PMID: 22339650]
[42]
Pérez-Jeldres T, Tyler CJ, Boyer JD, et al. Targeting cytokine signaling and lymphocyte traffic via small molecules in inflammatory bowel disease: JAK inhibitors and S1PR agonists. Front Pharmacol 2019; 10: 212.
[http://dx.doi.org/10.3389/fphar.2019.00212] [PMID: 30930775]
[43]
Winthrop KL. The emerging safety profile of JAK inhibitors in rheumatic disease. Nat Rev Rheumatol 2017; 13(4): 234-43.
[http://dx.doi.org/10.1038/nrrheum.2017.23] [PMID: 28250461]
[44]
Kang EH, Liao KP, Kim SC. Cardiovascular Safety of Biologics and JAK Inhibitors in Patients with Rheumatoid Arthritis. Curr Rheumatol Rep 2018; 20(7): 42.
[http://dx.doi.org/10.1007/s11926-018-0752-2] [PMID: 29846814]
[45]
Bollen L, Vande Casteele N, Ballet V, et al. Thromboembolism as an important complication of inflammatory bowel disease. Eur J Gastroenterol Hepatol 2016; 28(1): 1-7.
[http://dx.doi.org/10.1097/MEG.0000000000000495] [PMID: 26513610]
[46]
Sarlos P, Szemes K, Hegyi P, et al. Steroid but not biological therapy elevates the risk of venous thromboembolic events in inflammatory bowel disease: A meta-analysis. J Crohn’s Colitis 2018; 12(4): 489-98.
[http://dx.doi.org/10.1093/ecco-jcc/jjx162] [PMID: 29220427]
[47]
Bollen L, Vande Casteele N, Peeters M, et al. Short-term effect of infliximab is reflected in the clot lysis profile of patients with inflammatory bowel disease: a prospective study. Inflamm Bowel Dis 2015; 21(3): 570-8.
[http://dx.doi.org/10.1097/MIB.0000000000000301] [PMID: 25659086]
[48]
Detrez I, Thomas D, Van Steen K, et al. Successful Infliximab Treatment is Associated With Reversal of Clotting Abnormalities in Inflammatory Bowel Disease Patients. J Clin Gastroenterol 2019.
[http://dx.doi.org/10.1097/MCG.0000000000001290] [PMID: 31789759]
[49]
Scribano ML. Vedolizumab for inflammatory bowel disease: From randomized controlled trials to real-life evidence. World J Gastroenterol 2018; 24(23): 2457-67.
[http://dx.doi.org/10.3748/wjg.v24.i23.2457] [PMID: 29930467]
[50]
Danese S, Bonovas S, Peyrin-Biroulet L. Positioning ustekinumab in Crohn’s disease: From clinical evidence to clinical practice. J Crohn’s Colitis 2017; 11(10): 1258-66.
[http://dx.doi.org/10.1093/ecco-jcc/jjx079] [PMID: 28575273]
[51]
[52]
Panés J, Sandborn WJ, Schreiber S, et al. Tofacitinib for induction and maintenance therapy of Crohn’s disease: results of two phase IIb randomised placebo-controlled trials. Gut 2017; 66(6): 1049-59.
[http://dx.doi.org/10.1136/gutjnl-2016-312735] [PMID: 28209624]
[53]
Berekmeri A, Mahmood F, Wittmann M, Helliwell P. Tofacitinib for the treatment of psoriasis and psoriatic arthritis. Expert Rev Clin Immunol 2018; 14(9): 719-30.
[http://dx.doi.org/10.1080/1744666X.2018.1512404] [PMID: 30118353]
[54]
Sandborn WJ, Panés J, Sands BE, et al. Venous thromboembolic events in the tofacitinib ulcerative colitis clinical development programme. Aliment Pharmacol Ther 2019; 50(10): 1068-76.
[http://dx.doi.org/10.1111/apt.15514] [PMID: 31599001]
[55]
Verden A, Dimbil M, Kyle R, Overstreet B, Hoffman KB. Analysis of Spontaneous Postmarket Case Reports Submitted to the FDA Regarding Thromboembolic Adverse Events and JAK Inhibitors. Drug Saf 2018; 41(4): 357-61.
[http://dx.doi.org/10.1007/s40264-017-0622-2] [PMID: 29196988]
[56]
Desai RJ, Pawar A, Weinblatt ME, Kim SC. Comparative Risk of Venous Thromboembolism in Rheumatoid Arthritis Patients Receiving Tofacitinib Versus Those Receiving Tumor Necrosis Factor Inhibitors: An Observational Cohort Study. Arthritis Rheumatol 2019; 71(6): 892-900.
[http://dx.doi.org/10.1002/art.40798] [PMID: 30552833]
[57]
Markham A. Baricitinib: First Global Approval. Drugs 2017; 77(6): 697-704.
[http://dx.doi.org/10.1007/s40265-017-0723-3] [PMID: 28290136]
[58]
[59]
Taylor PC, Weinblatt ME, Burmester GR, et al. Cardiovascular Safety During Treatment With Baricitinib in Rheumatoid Arthritis. Arthritis Rheumatol 2019; 71(7): 1042-55.
[http://dx.doi.org/10.1002/art.40841] [PMID: 30663869]
[60]
D’Amico F, Fiorino G, Furfaro F, Allocca M, Danese S. Janus kinase inhibitors for the treatment of inflammatory bowel diseases: developments from phase I and phase II clinical trials. Expert Opin Investig Drugs 2018; 27(7): 595-9.
[http://dx.doi.org/10.1080/13543784.2018.1492547] [PMID: 29938545]
[61]
Duggan S, Keam SJ. Upadacitinib: First Approval. Drugs 2019; 79(16): 1819-28.
[http://dx.doi.org/10.1007/s40265-019-01211-z] [PMID: 31642025]
[62]
Genovese MC, Fleischmann R, Combe B, et al. Safety and efficacy of upadacitinib in patients with active rheumatoid arthritis refractory to biologic disease-modifying anti-rheumatic drugs (SELECT-BEYOND): a double-blind, randomised controlled phase 3 trial. Lancet 2018; 391(10139): 2513-24.
[http://dx.doi.org/10.1016/S0140-6736(18)31116-4] [PMID: 29908670]
[63]
Sandborn WJ, Ghosh S, Panes J, et al. Efficacy of Upadacitinib in a Randomized Trial of Patients With Active Ulcerative Colitis. Gastroenterology 2020; 158(8): 2139-2149.e14.
[http://dx.doi.org/10.1053/j.gastro.2020.02.030] [PMID: 32092309]
[64]
[65]
Xie W, Huang Y, Xiao S, Sun X, Fan Y, Zhang Z. Impact of Janus kinase inhibitors on risk of cardiovascular events in patients with rheumatoid arthritis: systematic review and meta-analysis of randomised controlled trials. Ann Rheum Dis 2019; 78(8): 1048-54.
[http://dx.doi.org/10.1136/annrheumdis-2018-214846] [PMID: 31088790]
[66]
Huang F, Luo ZC. Risk of Adverse Drug Events Observed with Baricitinib 2 mg Versus Baricitinib 4 mg Once Daily for the Treatment of Rheumatoid Arthritis: A Systematic Review and Meta-Analysis of Randomized Controlled Trials. BioDrugs 2018; 32(5): 415-23.
[http://dx.doi.org/10.1007/s40259-018-0304-3] [PMID: 30203252]
[67]
Xie W, Xiao S, Huang Y, Sun X, Zhang Z. Effect of tofacitinib on cardiovascular events and all-cause mortality in patients with immune-mediated inflammatory diseases: a systematic review and meta-analysis of randomized controlled trials. Ther Adv Musculoskelet Dis 2019; 11: X19895492.
[http://dx.doi.org/10.1177/1759720X19895492] [PMID: 31897092]
[68]
Razik R, Bernstein CN, Sam J, Thanabalan R, Nguyen GC. Survey of perceptions and practices among Canadian gastroenterologists regarding the prevention of venous thromboembolism for hospitalized inflammatory bowel disease patients. Can J Gastroenterol 2012; 26(11): 795-8.
[http://dx.doi.org/10.1155/2012/175249] [PMID: 23166902]
[69]
Sam JJ, Bernstein CN, Razik R, Thanabalan R, Nguyen GC. Physicians’ perceptions of risks and practices in venous thromboembolism prophylaxis in inflammatory bowel disease. Dig Dis Sci 2013; 58(1): 46-52.
[http://dx.doi.org/10.1007/s10620-012-2435-6] [PMID: 23053902]
[70]
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): e1-6.
[http://dx.doi.org/10.1097/MCG.0b013e31824c0dea] [PMID: 22476043]
[71]
Jackson BD, Con D, Liew D, De Cruz P. Clinicians’ adherence to international guidelines in the clinical care of adults with inflammatory bowel disease. Scand J Gastroenterol 2017; 52(5): 536-42.
[http://dx.doi.org/10.1080/00365521.2017.1278785] [PMID: 28128675]
[72]
Tsiolakidou G, Koutroubakis IE. Thrombosis and inflammatory bowel disease-the role of genetic risk factors. World J Gastroenterol 2008; 14(28): 4440-4.
[http://dx.doi.org/10.3748/wjg.14.4440] [PMID: 18680221]
[73]
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.e6.
[http://dx.doi.org/10.1053/j.gastro.2014.01.042] [PMID: 24462530]
[74]
Danese S, Argollo M, Le Berre C, Peyrin-Biroulet L. JAK selectivity for inflammatory bowel disease treatment: does it clinically matter? Gut 2019; 68(10): 1893-9.
[http://dx.doi.org/10.1136/gutjnl-2019-318448] [PMID: 31227590]
[75]
Lim W, Le Gal G, Bates SM, et al. American Society of Hematology 2018 guidelines for management of venous thromboembolism: diagnosis of venous thromboembolism. Blood Adv 2018; 2(22): 3226-56.
[http://dx.doi.org/10.1182/bloodadvances.2018024828] [PMID: 30482764]
[76]
Dentali F, Douketis JD, Gianni M, Lim W, Crowther MA. Meta-analysis: anticoagulant prophylaxis to prevent symptomatic venous thromboembolism in hospitalized medical patients. Ann Intern Med 2007; 146(4): 278-88.
[http://dx.doi.org/10.7326/0003-4819-146-4-200702200-00007] [PMID: 17310052]
[77]
Ananthakrishnan AN, Cagan A, Gainer VS, et al. Thromboprophylaxis is associated with reduced post-hospitalization venous thromboembolic events in patients with inflammatory bowel diseases. Clin Gastroenterol Hepatol 2014; 12(11): 1905-10.
[http://dx.doi.org/10.1016/j.cgh.2014.02.034] [PMID: 24632349]
[78]
Bryant RV, Jairath V, Curry N, Travis SP. Thrombosis in inflammatory bowel disease: are we tailoring prophylaxis to those most at risk? J Crohn’s Colitis 2014; 8(2): 166-71.
[http://dx.doi.org/10.1016/j.crohns.2013.09.007] [PMID: 24095288]
[79]
Wallaert JB, De Martino RR, Marsicovetere PS, et al. Venous thromboembolism after surgery for inflammatory bowel disease: are there modifiable risk factors? Data from ACS NSQIP. Dis Colon Rectum 2012; 55(11): 1138-44.
[http://dx.doi.org/10.1097/DCR.0b013e3182698f60] [PMID: 23044674]
[80]
Douketis JD, Spyropoulos AC, Spencer FA, et al. Perioperative management of antithrombotic therapy.Antithrombotic therapy and prevention of thrombosis, 9th ed. American College of Chest Physicians evidence-based clinical practice guidelines Chest 2012; 141: pp. e326-50.
[http://dx.doi.org/10.1378/chest.11-2298]
[81]
Gould MK, Karanicolas PJ, Garcia DA, et al. Prevention of VTE in Nonorthopedic Surgical Patients: Antithrombotic Therapy and Prevention of Thrombosis, 9th EdAmerican College of Chest Physicians Evidence-Based Clinical Practice Guidelines. Chest 2012; 141: pp. (2)e227-77.
[82]
Harbord M, Annese V, Vavricka SR, et al. European Crohn’s and Colitis Organisation. The first european evidence-based consensus on extra-intestinal manifestations in inflammatory bowel disease. J Crohn’s Colitis 2016; 10(3): 239-54.
[http://dx.doi.org/10.1093/ecco-jcc/jjv213] [PMID: 26614685]
[83]
Rubin DT, Ananthakrishnan AN, Siegel CA, Sauer BG, Long MD. ACG Clinical Guideline: Ulcerative Colitis in Adults. Am J Gastroenterol 2019; 114(3): 384-413.
[http://dx.doi.org/10.14309/ajg.0000000000000152] [PMID: 30840605]
[84]
Koutroumpakis EI, Tsiolakidou G, Koutroubakis IE. Risk of venous thromboembolism in patients with inflammatory bowel disease. Semin Thromb Hemost 2013; 39(5): 461-8.
[http://dx.doi.org/10.1055/s-0033-1343886] [PMID: 23629820]
[85]
Van Assche G, Dignass A, Bokemeyer B, et al. European Crohn’s and Colitis Organisation. Second European evidence-based consensus on the diagnosis and management of ulcerative colitis part 3: special situations. J Crohn’s Colitis 2013; 7(1): 1-33.
[http://dx.doi.org/10.1016/j.crohns.2012.09.005] [PMID: 23040453]
[86]
Dignass A, Van Assche G, Lindsay JO, et al. European Crohn’s and Colitis Organisation (ECCO). The second European evidence-based Consensus on the diagnosis and management of Crohn’s disease: Current management. J Crohn’s Colitis 2010; 4(1): 28-62.
[http://dx.doi.org/10.1016/j.crohns.2009.12.002] [PMID: 21122489]
[87]
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): 1486-95.
[http://dx.doi.org/10.1038/ajg.2013.220] [PMID: 23857476]
[88]
Ra G, Thanabalan R, Ratneswaran S, Nguyen GC. Predictors and safety of venous thromboembolism prophylaxis among hospitalized inflammatory bowel disease patients. J Crohn’s Colitis 2013; 7(10): e479-85.
[http://dx.doi.org/10.1016/j.crohns.2013.03.002] [PMID: 23537817]
[89]
Lewis JD, Scott FI, Brensinger CM, et al. Increased mortality rates with prolonged corticosteroid therapy when compared with antitumor necrosis factor-α-directed therapy for inflammatory bowel disease. Am J Gastroenterol 2018; 113(3): 405-17.
[http://dx.doi.org/10.1038/ajg.2017.479] [PMID: 29336432]
[90]
Singh S, Kullo IJ, Pardi DS, Loftus EV Jr. Epidemiology, risk factors and management of cardiovascular diseases in IBD. Nat Rev Gastroenterol Hepatol 2015; 12(1): 26-35.
[http://dx.doi.org/10.1038/nrgastro.2014.202] [PMID: 25446727]
[91]
Arnett DK, Blumenthal RS, Albert MA, et al. 2019 ACC/AHA Guideline on the Primary Prevention of Cardiovascular Disease: A Report of the American College of Cardiology/American Heart Association Task Force on Clinical Practice Guidelines. J Am Coll Cardiol 2019; 74(10): e177-232.
[http://dx.doi.org/10.1016/j.jacc.2019.03.010] [PMID: 30894318]

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