Use of azathioprine in IBD: Modern aspects of an old drug

Gut

Volumn 63, Issue 11, 2014, Pages 1695-1699

  Louis, Edouard ^a   Irving, Peter ^b   Beaugerie, Laurent ^c  

^a UNIVERSITY OF LIÈGE   (Belgium)

^b GUY'S AND ST THOMAS' NHS FOUNDATION TRUST   (United Kingdom)

^c HÔPITAL SAINT ANTOINE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ALLOPURINOL; AZATHIOPRINE; MERCAPTOPURINE; PLACEBO; IMMUNOSUPPRESSIVE AGENT;

ARTICLE; CLINICAL EFFECTIVENESS; CONCENTRATION (PARAMETERS); CROHN DISEASE; DISEASE SEVERITY; DRUG EFFICACY; DRUG METABOLISM; HUMAN; LYMPHOMA; OUTCOME ASSESSMENT; RECURRENT DISEASE; REMISSION; RISK ASSESSMENT; RISK BENEFIT ANALYSIS; RISK FACTOR; TREATMENT RESPONSE; ULCERATIVE COLITIS; COLITIS, ULCERATIVE; INFLAMMATORY BOWEL DISEASES; TREATMENT FAILURE;

AZATHIOPRINE; COLITIS, ULCERATIVE; CROHN DISEASE; HUMANS; IMMUNOSUPPRESSIVE AGENTS; INFLAMMATORY BOWEL DISEASES; REMISSION INDUCTION; TREATMENT FAILURE;

EID: 84907796504     PISSN: 00175749     EISSN: 14683288     Source Type: Journal    
DOI: 10.1136/gutjnl-2013-306711     Document Type: Article

References (66)

1. Prefontaine E, Sutherland LR, Macdonald JK, et al. Azathioprine or 6-mercaptopurine for maintenance of remission in Crohn's disease. Cochrane Database Syst Rev 2009;1:CD000067.
2. D'Haens G, Geboes K, Rutgeerts P. Endoscopic and histologic healing of Crohn's (ileo-) colitis with azathioprine. Gastrointest Endosc 1999;50:667-71.
3. Mantzaris GJ, Christidou A, Sfakianakis M, et al. Azathioprine is superior to budesonide in achieving and maintaining mucosal healing and histologic remission in steroid-dependent Crohn's disease. Inflamm Bowel Dis 2009;15:375-82.
4. Treton X, Bouhnik Y, Mary JY, et al. Azathioprine withdrawal in patients with Crohn's disease maintained on prolonged remission: a high risk of relapse. Clin Gastroenterol Hepatol 2009;7:80-5.
5. Ardizzone S, Maconi G, Russo A, et al. Randomised controlled trial of azathioprine and 5-aminosalicylic acid for treatment of steroid dependent ulcerative colitis. Gut 2006;55:47-53.
6. Timmer A, McDonald JW, Tsoulis DJ, et al. Azathioprine and 6-mercaptopurine for maintenance of remission in ulcerative colitis. Cochrane Database Syst Rev 2012;9:CD000478.
7. Cassinotti A, Actis GC, Duca P, et al. Maintenance treatment with azathioprine in ulcerative colitis: outcome and predictive factors after drug withdrawal. Am J Gastroenterol 2009;104:2760-7.
8. Ramadas AV, Gunesh S, Thomas GA, et al. Natural history of Crohn's disease in a population-based cohort from Cardiff (1986-2003): a study of changes in medical treatment and surgical resection rates. Gut 2010;59:1200-6.
9. Vernier-Massouille G, Balde M, Salleron J, et al. Natural history of pediatric Crohn's disease: a population-based cohort study. Gastroenterology 2008;135:1106-13.
10. Rungoe C, Langholz E, Andersson M, et al. Changes in medical treatment and surgery rates in inflammatory bowel disease: a nationwide cohort study 1979-2011. Gut 2014;63: 1607-16.
11. Cosnes J, Bourrier A, Laharie D, et al. Early administration of azathioprine vs conventional management of Crohn's Disease: a randomized controlled trial. Gastroenterology 2013;145:758-65.
12. Panés J, López-Sanromán A, Bermejo F, et al. Early azathioprine therapy is no more effective than placebo for newly diagnosed Crohn's disease. Gastroenterology 2013;145:766-74.
13. Colombel JF, Sandborn WJ, Reinisch W, et al. Infliximab, azathioprine, or combination therapy for Crohn's disease. N Engl J Med 2010;362:1383-95.
14. Panaccione R, Ghosh S, Middleton S, et al. Combination therapy with infliximab and azathioprine is superior to monotherapy with either agent in ulcerative colitis. Gastroenterology 2014;146:392-400.e3.pii: S0016-5085(13)01526-6.
15. Chatu S, Subramanian V, Saxena S, et al. The role of thiopurines in reducing the need for surgical resection in Crohn's disease. Am J Gastroenterol 2014;109:23-34.
16. Gisbert JP, Panés J. Loss of response and requirement of infliximab dose intensification in Crohn's disease: a review. Am J Gastroenterol 2009;104:760-7.
17. Sokol H, Seksik P, Carrat F, et al. Usefulness of co-treatment with immunomodulators in patients with inflammatory bowel disease treated with scheduled infliximab maintenance therapy. Gut 2010;59:1363-8.
18. Reenaers C, Louis E, Belaiche J, et al. Does co-treatment with immunosuppressors improve outcome in patients with Crohn's disease treated with adalimumab? Aliment Pharmacol Ther 2012;36:1040-8.
19. Dignass A, Van Assche G, Lindsay JO, et al. The second European evidence-based Consensus on the diagnosis and management of Crohn's disease: current management. J Crohn Colitis 2010;4:28-62.
20. Dervieux T, Boulieu R. Simultaneous determination of 6-thioguanine and methyl 6-mercaptopurine nucleotides of azathioprine in red blood cells by HPLC. Clin Chem 1998;44:551-5.
21. Moreau AC, Paul S, Del Tedesco E, et al. Association Between 6-Thioguanine Nucleotides Levels and Clinical Remission in Inflammatory Disease: a Meta-analysis. Inflamm Bowel Dis 2014;20:464-71.
22. Smith M, Blaker P, Patel C, et al. The impact of introducing thioguanine nucleotide monitoring into an inflammatory bowel disease clinic. Int J Clin Pract 2013;67:161-9.
23. Wright S, Sanders DS, Lobo AJ, et al. Clinical significance of azathioprine active metabolite concentrations in inflammatory bowel disease. Gut 2004;53:1123-8.
24. Hindorf U, Lyrenas E, Nilsson A, et al. Monitoring of long-term thiopurine therapy among adults with inflammatory bowel disease. Scand J Gastroenterol 2004;39:1105-12.
25. Gupta P, Gokhale R, Kirschner BS. 6-mercaptopurine metabolite levels in children with inflammatory bowel disease. J Pediatr Gastroenterol Nutr 2001;33:450-4.
26. Haines ML, Ajlouni Y, Irving PM, et al. Clinical usefulness of therapeutic drug monitoring of thiopurines in patients with inadequately controlled inflammatory bowel disease. Inflamm Bowel Dis 2011;17:1301-7.
27. Reinshagen M, Schutz E, Armstrong VW, et al. 6-thioguanine nucleotide-adapted azathioprine therapy does not lead to higher remission rates than standard therapy in chronic active crohn disease: results from a randomized, controlled, open trial. Clin Chem 2007;53:1306-14.
28. Dassopoulos T, Dubinsky MC, Bentsen JL, et al. Randomised clinical trial: individualised vs. weight-based dosing of azathioprine in Crohn's disease. Aliment Pharmacol Ther 2014;39: 163-75.
29. Blaker PA, Arenas-Hernandez M, Smith MA, et al. Mechanism of allopurinol induced TPMT inhibition. Biochem Pharmacol 2013;86:539-47.
30. Smith MA, Blaker P, Marinaki AM, et al. Optimising outcome on thiopurines in inflammatory bowel disease by co-prescription of allopurinol. J Crohn Colitis 2012;6:905-12.
31. Sparrow MP, Hande SA, Friedman S, et al. Effect of allopurinol on clinical outcomes in inflammatory bowel disease nonresponders to azathioprine or 6-mercaptopurine. Clin Gastroenterol Hepatol 2007;5:209-14.
32. Hoentjen F, Seinen ML, Hanauer SB, et al. Safety and effectiveness of long-term allopurinol-thiopurine maintenance treatment in inflammatory bowel disease. Inflamm Bowel Dis 2013;19:363-9.
33. Ansari A, Patel N, Sanderson J, et al. Low-dose azathioprine or mercaptopurine in combination with allopurinol can bypass many adverse drug reactions in patients with inflammatory bowel disease. Aliment Pharmacol Ther 2010;31:640-7.
34. Gearry RB, Barclay ML, Roberts RL, et al. Thiopurine methyltransferase and 6-thioguanine nucleotide measurement: early experience of use in clinical practice. Intern Med J 2005;35:580-5.
35. Connell WR, Kamm MA, Ritchie JK, et al. Bone marrow toxicity caused by azathioprine in inflammatory bowel disease: 27 years of experience. Gut 1993;34:1081-5.
36. O'Donoghue DP, Dawson AM, Powell-Tuck J, et al. Double-blind withdrawal trial of azathioprine as maintenance treatment for Crohn's disease. Lancet 1978;2:955-7.
37. Hou JK, Kramer JR, Richardson P, et al. Myelosuppression monitoring after immunomodulator initiation in veretans with inflammatory bowel disease: a national practice audit. Aliment Pharmacol Ther 2012;36:1049-56.
38. Gisbert JP, Gonzalez-Lama Y, Mate J. Thiopurine-induced liver injury in patients with inflammatory bowel disease: a systematic review. Am J Gastroenterol 2007;102:1518-27.
39. Seksik P, Mary JY, Beaugerie L, et al. Incidence of nodular regenerative hyperplasia in inflammatory bowel disease patients treated with azathioprine. Inflamm Bowel Dis 2011;17:565-72.
40. Toruner M, Loftus EV Jr, Harmsen WS, et al. Risk factors for opportunistic infections in patients with inflammatory bowel disease. Gastroenterology 2008;134:929-36.
41. Leung VS, Nguyen MT, Bush TM. Disseminated primary varicella after initiation of infliximab for Crohn's disease. Am J Gastroenterol 2004;99:2503-4.
42. Biank VF, Sheth MK, Talano J, et al. Association of Crohn's disease, thiopurines, and primary epstein-barr virus infection with hemophagocytic lymphohistiocytosis. J Pediatr 2011;159: 808-12.
43. Rahier JF, Ben-Horin S, Chowers Y, et al. European evidence based consensus on the prevention, diagnosis and management of opportunistic infections in IBD. J Crohn Colitis 2009;3:47-91.
44. Sokol H, Beaugerie L. Inflammatory bowel disease and lymphoproliferative disorders: the dust is starting to settle. Gut 2009;58:1427-36.
45. Beaugerie L, Brousse N, Bouvier AM, et al. Lymphoproliferative disorders in patients receiving thiopurines for inflammatory bowel disease: a prospective observational cohort study. Lancet 2009;374:1617-25.
46. Beaugerie L. Inflammatory bowel disease therapies and cancer risk: where are we and where are we going? Gut 2012;61:476-83.
47. Kinlen LJ, Sheil AG, Peto J, et al. Collaborative United Kingdom-Australasian study of cancer in patients treated with immunosuppressive drugs. Br Med J 1979;2:1461-6.
48. Pasternak B, Svanstrom H, Schmiegelow K, et al. Use of azathioprine and the risk of cancer in inflammatory bowel disease. Am J Epidemiol 2013;177:1296-305.
49. Beaugerie L, Carrat F, Colombel JF, et al. Risk of new or recurrent cancer under immunosuppressive therapy in patients with IBD and previous cancer. Gut 2014;63:1416-23.
50. Long MD, Martin CF, Pipkin CA, et al. Risk of melanoma and nonmelanoma skin cancer among patients with inflammatory bowel disease. Gastroenterology 2012;143:390-9.
51. Peyrin-Biroulet L, Khosrotehrani K, Carrat F, et al. Increased risk for nonmelanoma skin cancers in patients who receive thiopurines for inflammatory bowel disease. Gastroenterology 2011;141: 1621-8.
52. Singh H, Nugent Z, Demers AA, et al. Increased risk of non-melanoma skin cancers among individuals with inflammatory bowel disease. Gastroenterology 2011;141:1612-20.
53. Singh S, Nagpal SJ, Murad MH, et al. Inflammatory bowel disease is associated with an increased risk of melanoma: a systematic review and meta-analysis. Clin Gastroenterol Hepatol 2014;12:210-18.
54. Kane S. Abnormal Pap smears in inflammatory bowel disease. Inflamm Bowel Dis 2008;14:1158-60.
55. Lopez A, Mounier M, Bouvier AM, et al. Increased risk of acute myeloid leukemias and myelodysplastic syndromes in pateints with past exposure to thiopurines for Inflammatory Bowel Disase. Clin Gastroenterol hepatol 2014:pii: S1542-3565(14)00311-5. Published Online First: 26 Feb 2014. doi:10.1016/j.cgh.2014.02.026
56. Kotlyar DS, Osterman MT, Diamond RH, et al. A systematic review of factors that contribute to hepatosplenic T-cell lymphoma in patients with inflammatory bowel disease. Clin Gastroenterol Hepatol 2011;9:36-41.
57. Khan N, Abbas AM, Lichtenstein GR, et al. Risk of lymphoma in patients with ulcerative colitis treated with thiopurines: a nationwide retrospective cohort study. Gastroenterology 2013;145:1007-15.
58. Kandiel A, Fraser AG, Korelitz BI, et al. Increased risk of lymphoma among inflammatory bowel disease patients treated with azathioprine and 6-mercaptopurine. Gut 2005;54:1121-5.
59. Hutfless SM, Weng X, Liu L, et al. Mortality by medication use among patients with inflammatory bowel disease, 1996-2003. Gastroenterology 2007;133:1779-86.
60. Lewis JD, Gelfand JM, Troxel AB, et al. Immunosuppressant medications and mortality in inflammatory bowel disease. Am J Gastroenterol 2008;103:1428-35.
61. Jess T, Frisch M, Simonsen J. Trends in overall and cause-specific mortality among patients with inflammatory bowel disease from 1982 to 2010. Clin Gastroenterol Hepatol 2013;11:43-8.
62. Lewis JD, Schwartz JS, Lichtenstein GR. Azathioprine for maintenance of remission in Crohn's disease: benefits outweigh the risk of lymphoma. Gastroenterology 2000;118:1018-24.
63. Charpentier C, Salleron J, Savoye G, et al. Natural history of elderly-onset inflammatory bowel disease: a population-based cohort study. Gut 2014;63:423-32.
64. Lichtenstein GR, Feagan BG, Cohen RD, et al. Serious infections and mortality in association with therapies for Crohn's disease: TREAT registry. Clin Gastroenterol Hepatol 2006;4:621-30.
65. Cottone M, Kohn A, Daperno M, et al. Advanced age is an independent risk factor for severe infections and mortality in patients given anti-tumor necrosis factor therapy for inflammatory bowel disease. Clin Gastroenterol Hepatol 2011;9:30-5.
66. Johnson FR, Ozdemir S, Mansfield C, et al. Crohn's disease patients' risk-benefit preferences: serious adverse event risks versus treatment efficacy. Gastroenterology 2007;133:769-79.