Is there an increased risk of lymphoma and malignancies under anti-TNF therapy in IBD?

Current Drug Targets

Volumn 11, Issue 2, 2010, Pages 179-186

  Lakatos, P L ^a   Miheller, P ^a  

^a SEMMELWEIS UNIVERSITY   (Hungary)

Author keywords

Adalimumab; Anti TNF; CD; Certolizumab; HSTCL; IBD; Infliximab; Lymphoma; Malignancy; UC

Indexed keywords

AZATHIOPRINE; ENDOTHELIAL LEUKOCYTE ADHESION MOLECULE 1; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; IMMUNOSUPPRESSIVE AGENT; INTERCELLULAR ADHESION MOLECULE 1; INTERLEUKIN 1BETA; INTERLEUKIN 6; INTERLEUKIN 8; MACROPHAGE INFLAMMATORY PROTEIN; MACROPHAGE INFLAMMATORY PROTEIN 1ALPHA; METHOTREXATE; MONOCYTE CHEMOTACTIC PROTEIN 1; RANTES; TUMOR NECROSIS FACTOR ALPHA; TUMOR NECROSIS FACTOR ANTIBODY; TUMOR NECROSIS FACTOR RECEPTOR 1; TUMOR NECROSIS FACTOR RECEPTOR 2; VASCULAR CELL ADHESION MOLECULE 1;

CANCER INCIDENCE; CANCER RISK; CANCER THERAPY; CARCINOGENESIS; CROHN DISEASE; ENTERITIS; HUMAN; IMMUNOMODULATION; LYMPHOMA; NONHODGKIN LYMPHOMA; NONHUMAN; REVIEW; T CELL LYMPHOMA; VIRUS INFECTION;

ANIMALS; ANTI-INFLAMMATORY AGENTS; DRUG DELIVERY SYSTEMS; HUMANS; IMMUNOSUPPRESSIVE AGENTS; INFLAMMATORY BOWEL DISEASES; LYMPHOMA; NEOPLASMS; TUMOR NECROSIS FACTOR-ALPHA;

EID: 77950833122     PISSN: 13894501     EISSN: None     Source Type: Journal    
DOI: 10.2174/138945010790309867     Document Type: Review

References (76)

1. Lakatos PL, Fischer S, Lakatos L, Gal I, Papp J. Current concept on the pathogenesis of inflammatory bowel disease-crosstalk between genetic and microbial factors: pathogenic bacteria and altered bacterial sensing or changes in mucosal integrity take "toll"? World J Gastroenterol 2006; 12: 1829-1841.
2. Lakatos PL. Recent trends in the epidemiology of inflammatory bowel diseases: up or down? World J Gastroenterol 2006; 12: 6102-6108 (Pubitemid 44688157)
3. Faubion WA Jr, Loftus EV Jr. Harmsen WS, Zinsmeister AR, Sandborn WJ. The natural history of corticosteroid therapy for inflammatory bowel disease: a population-based study. Gastroenterology 2001; 121: 255-260 (Pubitemid 32729372)
4. Hanauer SB, Feagan BG, Lichtenstein GR, Mayer LF, Schreiber S, Colombel J, et al. Maintenance infliximab for Crohn's disease: the ACCENT I randomised trial. Lancet 2002; 359: 1541-1549 (Pubitemid 34621118)
5. Sands BE, Anderson FH, Bernstein CN, Chey WY, Feagan BG, Fedorak RN, et al. Infliximab maintenance therapy for fistulizing Crohn's disease. N Engl J Med 2004; 350: 876-885
6. Hanauer SB, Sandborn WJ, Rutgeerts P, Fedorak RN, Lukas M, MacIntosh D, et al. Human anti-tumour necrosis factor monoclonal antibody (adalimumab) in Crohn's disease: the CLASSIC-I trial. Gastroenterology 2006; 130: 323-333
7. Sandborn WJ, Hanauer SB, Rutgeerts P, Fedorak RN, Lukas M, MacIntosh DG, et al. Adalimumab for maintenance treatment of Crohn's disease: results of the CLASSIC II trial. Gut 2007; 56: 1232-1239 (Pubitemid 47300424)
8. Colombel JF, Sandborn WJ, Rutgeerts P, Enns R, Hanauer SB, Panaccione R, et al. Adalimumab for maintenance of clinical response and remission in patients with Crohn's disease: the CHARM trial. Gastroenterology 2007; 132: 52-65. (Pubitemid 46108762)
9. Sandborn WJ, Feagan BG, Stoinov S, Honiball PJ, Rutgeerts P, Mason D, et al. Certolizumab pegol for the treatment of Crohn's disease. N Engl J Med 2007; 357: 228-238 (Pubitemid 47080387)
10. Schreiber S, Khaliq-Kareemi M, Lawrance IC, Thomsen OO, Hanauer SB, McColm J, et al. Maintenance therapy with certolizumab pegol for Crohn's disease. N Engl J Med 2007; 357: 239-250 (Pubitemid 47080388)
11. Rutgeerts P, Sandborn WJ, Feagan BG, Reinisch W, Olson A, Johanns J, et al. Infliximab for induction and maintenance therapy for ulcerative colitis. N Engl J Med 2005; 353: 2462-2476 (Pubitemid 41770166)
12. Kotlyar D, Blonski, W, Mendizabal, M, Lin, MV, Weiner, M, Lichtenstein GR. Increased Risk of Lymphoma in the Setting of IBD: Prevalence Over a Decade in a Tertiary Academic Medical Gastroenterology 2009; 136(Suppl 1): S1148.
13. Roach DR, Bean AG, Demangel C, France MP, Briscoe H, Britton WJ. TNF regulates chemokine induction essential for cell recruitment, granuloma formation, and clearance of mycobacterial infection. J Immunol 2002; 168: 4620-4627 (Pubitemid 34441368)
14. Danese S. Mechanism of action of infliximab in inflammatory bowel disease: an anti-inflammatory multitasker. Dig Liver Dis 2008; 40(Suppl 2): S225-8.
15. Rosenberg SA, Yang JC, Schwartzentruber DJ, Hwu P, Marincola FM, Topalian SL, et al. Immunologic and therapeutic evaluation of a synthetic peptide vaccine for the treatment of patients with metastatic melanoma. Nat Med 1998; 4: 321-327
16. Micheau O, Tschopp J. Induction of TNF receptor I-mediated apoptosis via two sequential signaling complexes. Cell 2003; 114: 181-190
17. Popivanova BK, Kitamura K, Wu Y, Kondo T, Kagaya T, Kaneko S, et al. Blocking TNF-alpha in mice reduces colorectal carcinogenesis associated with chronic colitis. J Clin Invest 2008; 118: 560-570
18. Soderlund S, Brandt L, Lapidus A, Karlen P, Brostrom O, Lofberg R, et al. Decreasing time-trends of colorectal cancer in a large cohort of patients with inflammatory bowel disease. Gastroenterology 2009; 136: 1561-1567
19. Lakatos L, Mester G, Erdelyi Z, David G, Pandur T, Balogh M, et al. Risk factors for ulcerative colitis-associated colorectal cancer in a Hungarian cohort of patients with ulcerative colitis: results of a population-based study. Inflamm Bowel Dis 2006; 12: 205-211
20. Sachar DB. Cancer in Crohn's disease: dispelling the myths. Gut 1994; 35: 1507-1508
21. Bernstein CN, Blanchard JF, Kliewer E, Wajda A. Cancer risk in patients with inflammatory bowel disease: a population-based study. Cancer 2001; 91: 854-862
22. Rubio CA, Befrits R. Colorectal cancer in Crohn's disease -- Review of a 56-year experience in Karolinska Institute University Hospital. J Environ Pathol Toxicol Oncol 2008; 27: 257-266
23. Beaugerie L, Seksik, P, Carrat, F for the CESAME Study Group. Thiopurine Therapy Is Associated with a Three-Fold Decrease in the incidence of advanced colorectal neoplasia in ibd patients with longstanding extensive colitis: Results from the CESAME Cohort J Crohn's Colitis 2009; 3: S5-6
24. Alexander DD, Mink PJ, Adami HO, Chang ET, Cole P, Mandel JS, et al. The non-Hodgkin lymphomas: a review of the epidemiologic literature. Int J Cancer 2007; 120(Suppl12): 1-39 (Pubitemid 46732571)
25. Fisher SG, Fisher RI. The epidemiology of non-Hodgkin's lymphoma. Oncogene 2004; 23: 6524-6534
26. Baecklund E, Iliadou A, Askling J, Ekbom A, Backlin C, Granath F, et al. Association of chronic inflammation, not its treatment, with increased lymphoma risk in rheumatoid arthritis. Arthritis Rheum 2006; 54: 692-701.
27. Silman AJ, Petrie J, Hazleman B, Evans SJ. Lymphoproliferative cancer and other malignancy in patients with rheumatoid arthritis treated with azathioprine: a 20 year follow up study. Ann Rheum Dis 1988; 47: 988-992
28. Wilkinson AH, Smith JL, Hunsicker LG, Tobacman J, Kapelanski DP, Johnson M, et al. Increased frequency of posttransplant lymphomas in patients treated with cyclosporine, azathioprine, and prednisone. Transplantation 1989; 47: 293-296 (Pubitemid 19069708)
29. Reijasse D, Le Pendeven C, Cosnes J, Dehee A, Gendre JP, Nicolas JC, et al. Epstein-Barr virus viral load in Crohn's disease: effect of immunosuppressive therapy. Inflamm Bowel Dis 2004; 10: 85-90.
30. Copie-Bergman C, Niedobitek G, Mangham DC, Selves J, Baloch K, Diss TC, et al. Epstein-Barr virus in B-cell lymphomas associated with chronic suppurative inflammation. J Pathol 1997; 183: 287-292
31. Knosel T, Schewe C, Petersen N, Dietel M, Petersen I. Prevalence of infectious pathogens in Crohn's disease. Pathol Res Pract 2009; 205: 223-230
32. Wong NA, Herbst H, Herrmann K, Kirchner T, Krajewski AS, Moorghen M, et al. Epstein-Barr virus infection in colorectal neoplasms associated with inflammatory bowel disease: detection of the virus in lymphomas but not in adenocarcinomas. J Pathol 2003; 201: 312-318
33. Dayharsh GA, Loftus EV, Jr., Sandborn WJ, Tremaine WJ, Zinsmeister AR, Witzig TE, et al. Epstein-Barr virus-positive lymphoma in patients with inflammatory bowel disease treated with azathioprine or 6-mercaptopurine. Gastroenterology 2002; 122: 72-77
34. Vos C, Bakkal N, Minnee RC, De Jong DJ, Dijkstra G, Stokkers P, et al. Increased risk of lymphoma among inflammatory bowel disease patients treated with azathioprine in a Dutch Nationwide study. Gastroenterology 2009; 136(Suppl 1): S1031.
35. Lewis JD, Bilker WB, Brensinger C, Deren JJ, Vaughn DJ, Strom BL. Inflammatory bowel disease is not associated with an increased risk of lymphoma. Gastroenterology 2001; 121: 1080-1087
36. Ekbom A, Helmick C, Zack M, Adami HO. Extracolonic malignancies in inflammatory bowel disease. Cancer 1991; 67: 2015-2019
37. Loftus EV Jr, Tremaine WJ, Habermann TM, Harmsen WS, Zinsmeister AR, Sandborn WJ. Risk of lymphoma in inflammatory bowel disease. Am J Gastroenterol 2000; 95: 2308-2312
38. Persson PG, Karlen P, Bernell O, Leijonmarck CE, Brostrom O, Ahlbom A, et al. Crohn's disease and cancer: a population-based cohort study. Gastroenterology 1994; 107: 1675-1679
39. Askling J, Brandt L, Lapidus A, Karlen P, Bjorkholm M, Lofberg R, et al. Risk of haematopoietic cancer in patients with inflammatory bowel disease. Gut 2005; 54: 617-622
40. Kandiel A, Fraser AG, Korelitz BI, Brensinger C, Lewis JD. Increased risk of lymphoma among inflammatory bowel disease patients treated with azathioprine and 6-mercaptopurine. Gut 2005; 54: 1121-1125
41. Beaugerie L, Carrat F, Bouvier AM, Brousse N, Carbonnel F, Colombel JF, et al. Excess risk of lymphoproliferative disorders (Lpd) in inflammatory bowel diseases (IBD): interim results of the cesame cohort. Gastroenterology 2008; 134 (Suppl 1): 818.
42. Farrell RJ, Ang Y, Kileen P, O'Briain DS, Kelleher D, Keeling PW, et al. Increased incidence of non-Hodgkin's lymphoma in inflammatory bowel disease patients on immunosuppressive therapy but overall risk is low. Gut 2000; 47: 514-519
43. Kane S, Khatibi B, Reddy D. Higher incidence of abnormal Pap smears in women with inflammatory bowel disease. Am J Gastroenterol 2008; 103: 631-636
44. Hutfless S, Fireman B, Kane S, Herrinton LJ. Screening differences and risk of carvical cancer in inflammatory bowel disease. Aliment Pharmacol Ther 2008; 28: 598-605.
45. Singh H, Demers AA, Nugent Z, Mahmud SM, Kliewer EV, Bernstein CN. Risk of cervical abnormalities in women with inflammatory bowel disease: A population-based nested casecontrol study. Gastroenterology 2009; 136: 451-458
46. Lees CW, Critchley J, Chee N, Beez T, Gailer RE, Williams AR, et al. Lack of association between cervical dysplasia and IBD: A large case-control study. Inflamm Bowel Dis 2009; 15: 1621-1629
47. Bongartz T, Sutton AJ, Sweeting MJ, Buchan I, Matteson EL, Montori V. Anti-TNF antibody therapy in rheumatoid arthritis and the risk of serious infections and malignancies: systematic review and meta-analysis of rare harmful effects in randomized controlled trials. JAMA 2006; 295: 2275-2285
48. Askling J, Klareskog L, Hjalgrim H, Baecklund E, Bjorkholm M, Ekbom A. Do steroids increase lymphoma risk? A case-control study of lymphoma risk in polymyalgia rheumatica/giant cell artheritis. Ann Rheum Dis 2005; 64: 1765-1768
49. Behm B. Bickston SJ. Tumour necrosis factor-alpha antibody for maintenace of remission in Crohn's disease. Cohrane Database Syst Rev 2008; 23: CD006893.
50. Lichtenstein GR, Feagan BG, Cohen RD, Salzberg BA, Diamond RH, Chen DM, et al. Serious infections and mortality in association with therapies for Crohn's disease: TREAT registry. Clin Gastroenterol Hepatol 2006; 4: 621-630
51. Peyrin-Biroulet L, Deltenre P, de Suray N, Branche J, Sandborn WJ, Colombel JF. Efficacy and safety of tumour necrosis factor antagonists in Crohn's disease: meta-analysis of placebo controlled trials. Clin Gastroenterol Hepatol 2008; 6: 644-653
52. Fidder H, Schnitzler F, Ferrante M, Noman M, Katsanos K, Segaert S, et al. Long-term safety of infliximab for the treatment of inflammatory bowel disease: a single-centre cohort study. Gut 2009; 58: 501-508
53. Onizawa M, Nagaishi T, Kanai T, Nagano K, Oshima S, Nemoto Y, et al. Signaling pathway via TNF-alpha/NF-kappaB in intestinal epithelial cells may be directly involved in colitis-associated carcinogenesis. Am J Physiol Gastrointest Liver Physiol 2009; 296: G850-9
54. ColombelJ, Sandborn WJ, Panaccione R, Robinson AM, Lau W, Lu J, et al. Adalimumab safety in global clinical trials. Inflamm Bowel Dis 2009; 15: 1308-1319
55. th of July2009www.fda.gov/ohrms/dockets/ac/03/briefing/3930B1-01- B-TNF.Briefing.htm.
56. Mellemkjaer L, Linet MS, Gridley G, Frisch M, Moller H, Olsen JH. Rheumatoid arthritis and cancer risk. Eur J Cancer 1996; 32A: 1753-1757
57. Thomas E, Brewster DH, Black RJ, Macfarlane GJ. Risk of malignancy among patients with rheumatic conditions. Int J Cancer 2000; 88: 497-502
58. Askling J, Fored CM, Baecklund E, Brandt L, Backlin C, Ekbom A, et al. Haematopoietic malignancies in rheumatoid arthritis: lymphoma risk and characteristics after exposure to tumour necrosis factor antagonists. Ann Rheum Dis 2005; 64: 1414-1420 (Pubitemid 41623850)
59. Askling J, Baecklund E, Granath F, Geborek P, Fored M, Backlin C, et al. Anti-tumour necrosis factor therapy in rheumatoid arthritis and risk of malignant lymphomas: Relative risk and time trends in the Swedish Biologics Register. Ann Rheum Dis 2009; 68: 648-653
60. Colombel JF, Loftus EV, Jr., Tremaine WJ, Egan LJ, Harmsen WS, Schleck CD, et al. The safety profile of infliximab in patients with Crohn's disease: the Mayo clinic experience in 500 patients. Gastroenterology 2004; 126: 19-31
61. Siegel CA, Marden SM, Persing SM, Larson RJ, Sands BE. Risk of lymphoma associated with combination anti-tumour necrosis factor and immunomodulator therapy for the treatment of Crohn's disease: a meta-analysis. Clin Gastroenterol Hepatol 2009; 7: 874-881
62. Colombel J, Schreiber S, Hanauer SB, Rutgeerts P, Sandborn WJ. Long-term tolerability of subcutaneous certolizumab pegol in active Crohn's disease:results from precise 3 and 4. Gastroenterology 2007; 132: A503
63. Mantzaris GJ, Sfakianakis M, Archavlis E, Petraki K, Christidou A, Karagiannidis A, et al. A prospective randomized observer-blind 2-year trial of azathioprine monotherapy versus azathioprine and olsalazine for the maintenance of remission of steroid-dependent ulcerative colitis. Am J Gastroenterol 2004; 99: 1122-1128
64. Rutgeerts P, D'Haens G, Targan S, Vasiliauskas E, Hanauer SB, Present DH, et al. Efficacy and safety of retreatment with antitumour necrosis factor antibody (infliximab) to maintain remission in Crohn's disease. Gastroenterology 1999; 117: 761-769
65. Biancone L, Orlando A, Kohn A, Colombo E, Sostegni R, Angelucci E, et al. Infliximab and newly diagnosed neoplasia in Crohn's disease: a multicentre matched pair study. Gut 2006; 55: 228-233
66. Lichtenstein GR, Cohen RD, Feagan BG, Sandborn WJ, Salzberg, BA, Chen DM, et al. Greater exposure to infliximab is not associated with increased mortality and serious infections- Treat registry data with nearly 20,000 patient-years of follow-up. Gastroenterology 2007; 132(supplS): A178.
67. Cohen R. Efficacy and safety of repeated infliximab infusions for Crohn's disease: 1-year clinical experience. Inflamm Bowel Dis 2001; 7: S17-22.
68. Kinney T, Rawlins M, Kozarek R, France R, Patterson D. Immunomodulators and "on demand" therapy with infliximab in Crohn's disease: clinical experience with 400 infusions. Am J Gastroenterol 2003; 98: 608-612 (Pubitemid 36348533)
69. Ljung T, Karlen P, Schmidt D, Hellstrom PM, Lapidus A, Janczewska I, et al. Infliximab in inflammatory bowel disease: clinical outcome in a population based cohort from Stockholm County. Gut 2004; 53: 849-853 (Pubitemid 38662135)
70. Seiderer J, Goke B, Ochsenkuhn T. Safety aspects of infliximab in inflammatory bowel disease patients. A retrospective cohort study in 100 patients of a German University Hospital. Digestion 2004; 70: 3-9.
71. Shale M, Kanfer E, Panaccione R, Ghosh S. Hepatosplenic T cell lymphoma in inflammatory bowel disease. Gut 2008; 57: 1639-1641
72. Zeidan A, Sham R, Shapiro J, Baratta A, Kouides P. Hepatosplenic T-cell lymphoma in a patient with Crohn's disease who received infliximab therapy. Leuk Lymphoma 2007; 48: 1410-1413 (Pubitemid 47079370)
73. Kotlyar D, Blonski W, Porter DL, Mendizabal M, Lin MV, Lichtenstein GR. Hepatosplenic T-Cell Lymphoma (HSTCL) and Inflammatory Bowel Disease (IBD): a Rare Complication After Long-Term Thiopurine Exposure: Case Report and Systematic Review of the Literature. Gastroenterology 2009; 136(SupplS): S1133.
74. Toruner M, Loftus EV Jr, Harmsen WS, Zinsmeister AR, Orenstein R, Sandborn WJ, et al. Risk factors for opportunistic infections in patients with inflammatory bowel disease. Gastroenterology 2008; 134: 929-936 (Pubitemid 351451967)
75. Moran G, Dillon J, Green J. Crohn's disease, hepatosplenic T-cell lymphoma and no biological therapy: Are we barking up the wrong tree? Inflamm Bowel Dis 2009; 15: 1281-1282
76. Rosh JR, Gross T, Mamula P, Griffiths A, Hyams J. Hepatosplenic T-cell lymphoma in adolescents and young adults with Crohn's disease: a cautionary tale? Inflamm Bowel Dis 2007; 13: 1024-1030