Review article: Non-malignant haematological complications of anti-tumour necrosis factor alpha therapy

Alimentary Pharmacology and Therapeutics

Volumn 36, Issue 4, 2012, Pages 312-323

  Bessissow, T ^a,b   Renard, M ^a   Hoffman, I ^a   Vermeire, S ^a   Rutgeerts, P ^a   Van Assche, G ^a  

^a UNIVERSITY HOSPITALS LEUVEN   (Belgium)

^b ROYAL VICTORIA HOSPITAL   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ADALIMUMAB; AZATHIOPRINE; CARDIOLIPIN ANTIBODY; DISEASE MODIFYING ANTIRHEUMATIC DRUG; ETANERCEPT; GLUCOCORTICOID; IMMUNOGLOBULIN; IMMUNOGLOBULIN A; IMMUNOGLOBULIN G; IMMUNOGLOBULIN M; INFLIXIMAB; MERCAPTOPURINE; MESALAZINE; METHOTREXATE; PREDNISONE; SALAZOSULFAPYRIDINE; STEROID; TUMOR NECROSIS FACTOR ALPHA INHIBITOR;

ANKYLOSING SPONDYLITIS; ANTIBODY DETECTION; APLASTIC ANEMIA; CELL DIFFERENTIATION; COHORT ANALYSIS; CROHN DISEASE; CYTOKINE PRODUCTION; DISEASE SEVERITY; DRUG EFFICACY; DRUG EXPOSURE; DRUG SAFETY; DRUG WITHDRAWAL; ENTERITIS; EOSINOPHIL COUNT; HEMATOPOIESIS; HUMAN; HYPERCOAGULABILITY; IDIOPATHIC THROMBOCYTOPENIC PURPURA; IMMUNOGLOBULIN BLOOD LEVEL; INSULIN RESISTANCE; JUVENILE RHEUMATOID ARTHRITIS; LEUKOCYTE COUNT; LEUKOPENIA; NEUTROPENIA; NEUTROPHIL COUNT; PANCYTOPENIA; PATHOGENESIS; POSTMARKETING SURVEILLANCE; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; PSORIASIS; PSORIATIC ARTHRITIS; REVIEW; RHEUMATOID ARTHRITIS; SACROILIITIS; SARCOIDOSIS; SCLERODERMA; SPONDYLOARTHROPATHY; SYSTEMATIC REVIEW; SYSTEMIC LUPUS ERYTHEMATOSUS; T LYMPHOCYTE; THROMBOCYTE AGGREGATION; THROMBOCYTE COUNT; THROMBOCYTOPENIA; THROMBOSIS; TREATMENT RESPONSE; ULCERATIVE COLITIS; UPREGULATION;

ANEMIA; BLOOD PLATELET DISORDERS; EOSINOPHILIA; HEMATOLOGIC DISEASES; HUMANS; NEUTROPENIA; THROMBOSIS; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84863989548     PISSN: 02692813     EISSN: 13652036     Source Type: Journal    
DOI: 10.1111/j.1365-2036.2012.05189.x     Document Type: Review

References (94)

1. Bradley JR,. TNF-mediated inflammatory disease. J Pathol 2008; 214: 149-60.
2. Breese EJ, Michie CA, Nicholls SW, et al,. Tumor necrosis factor alpha-producing cells in the intestinal mucosa of children with inflammatory bowel disease. Gastroenterology 1994; 106: 1455-66.
3. Lichtenstein GR, Hanauer SB, Sandborn WJ,. Practice Parameters Committee of American College of Gastroenterology. Management of Crohn's disease in adults. Am J Gastroenterol 2009; 104: 465-83.
4. Haraoui B,. Differentiating the efficacy of the tumor necrosis factor inhibitors. Semin Arthritis Rheum 2005; 34 (Suppl. 1): 7-11.
5. Miehsler W, Novacek G, Wenzl H, et al,. Austrian Society of Gastroenterology and Hepatology. A decade of infliximab: the Austrian evidence based consensus on the safe use of infliximab in inflammatory bowel disease. J Crohns Colitis 2010; 4: 221-56.
6. Furst DE, Schiff MH, Fleischmann RM, et al,. Adalimumab, a fully human anti tumor necrosis factor-alpha monoclonal antibody, and concomitant standard antirheumatic therapy for the treatment of rheumatoid arthritis: results of STAR (Safety Trial of Adalimumab in Rheumatoid Arthritis). J Rheumatol 2003; 30: 2563-71.
7. Ang HT, Helfgott S,. Do the clinical responses and complications following etanercept or infliximab therapy predict similar outcomes with the other tumor necrosis factor-α antagonists in patients with rheumatoid arthritis? J Rheumatol 2003; 30: 2315-8.
8. Feltelius N, Fored CM, Blomqvist P, et al,. ARTIS Group. Results from a nationwide postmarketing cohort study of patients in Sweden treated with etanercept. Ann Rheum Dis 2005; 64: 246-52.
9. Jacobsen SE, Jacobsen FW, Fahlman C, Rusten LS,. TNF-alpha, the great imitator: role of p55 and p75 TNF receptors in hematopoiesis. Stem Cells 1994; 12 (Suppl. 1): 111-26.
10. Keystone EC,. Tumor necrosis factor-alpha blockade in the treatment of rheumatoid arthritis. Rheum Dis Clin North Am 2001; 27: 427-43.
11. Andres E, Dali-Youcef N, Serraj K, Zimmer J,. Recognition and management of drug-induced cytopenias: the example of idiosyncratic drug-induced thrombocytopenia. Expert Opin Drug Saf 2009; 8: 183-90.
12. Visentin GP, Liu CY,. Drug-induced thrombocytopenia. Hematol Oncol Clin North Am 2007; 21: 685-96.
13. Chen M, Holland MJ, Mir MR, et al,. Frequency of thrombocytopenia in psoriasis patients treated with tumor necrosis factor-a inhibitors. J Drugs Dermatol 2011; 10: 280-4.
14. Brunasso AM, Massone C,. Thrombocytopenia associated with the use of anti-tumor necrosis factor-alpha agents for psoriasis. J Am Acad Dermatol 2009; 60: 781-5.
15. Data on file, Crohn's Disease Integrated Summary of Safety, Abbott, Montreal, Canada.
16. Data on file, Rheumatoid Arthritis Integrated Summary of Safety, Abbott, Montreal, Canada.
17. Data on file (S-AE-63-D2, 2006), Janssen Biotech, Inc., Horsham, PA, USA.
18. Data on file (ISS; pages 134-136, 2005), Centocor, Inc., Horsham, PA, USA.
19. Data on file (Protocol C0168T47; 2004), Janssen Biotech, Inc., Horsham, PA, USA.
20. Selby LA, Hess D, Shashidar H, de Villiers WJ, Selby LA,. Crohn's disease, infliximab and idiopathic thrombocytopenic purpura. Inflamm Bowel Dis 2004; 10: 698-700.
21. Hamaguchi M, Kawahito Y, Ishino H, Yoshida M, Yoshikawa T,. A case report of tumor necrosis factor-alpha antibody-induced thrombocytopenia associated with emerging IgM anticardiolipin antibody in patients with scleroderma overlap/rheumatoid arthritis. Clin Rheumatol 2007; 26: 988-90.
22. Vidal F, Fontova R, Richart C,. Severe neutropenia and thrombocytopenia associated with infliximab. Ann Intern Med 2003 5; 139: W-W63.
23. Feletar M, Brockbank JE, Schentag CT, Lapp V, Gladman DD,. Treatment of refractory psoriatic arthritis with infliximab: a 12 month observational study of 16 patients. Ann Rheum Dis 2004; 63: 156-61.
24. Pathare SK, Heycock C, Hamilton J,. TNFalpha blocker-induced thrombocytopenia. Rheumatology (Oxford) 2006; 45: 1313-4.
25. Salar A, Bessa X, Muñiz E, Monfort D, Besses C, Andreu M,. Infliximab and adalimumab-induced thrombocytopenia in a woman with colonic Crohn's disease. Gut 2007; 56: 1169-70.
26. Lahbabi I, Adamski H, Le Jean S, Cannieux V, Polard E, Chevrant-Breton J,. Neutropenia and thrombocytopenia in a patient presenting psoriasis treated with etanercept. Ann Dermatol Venereol 2008; 135: 409-10.
27. Stinco G, Piccirillo F, Patrone P,. Transient and slight thrombocytopaenia induced by etanercept during treatment of psoriatic arthritis. Acta Derm Venereol 2008; 88: 281-2.
28. Gerloni V, Pontikaki I, Gattinara M, Fantini F,. Focus on adverse events of tumour necrosis factor alpha blockade in juvenile idiopathic arthritis in an open monocentric long-term prospective study of 163 patients. Ann Rheum Dis 2008; 67: 1145-52.
29. Balato N, Gallo L, Gaudiello F, Chiurazzi F, Ayala F,. Transient and reversible thrombocytopenia in a psoriatic patient treated with etanercept. J Dermatolog Treat 2010; 21: 117-8.
30. Mocciaro F, Russo G, Di Mitri R, Marino A,. Infliximab-induced thrombocytopenia in an elderly patient with ileocolonic crohn's disease. Inflamm Bowel Dis 2012 [Epub ahead of print].
31. Capsoni F, Sarzi-Puttini P, Zanella A,. Primary and secondary autoimmune neutropenia. Arthritis Res Ther 2005; 7: 208e14.
32. Van der Klauw MM, Goudsmit R, Halie MR, et al,. A population-based case-cohort study of drug-associated agranulocytosis. Arch Intern Med 1999; 159: 369-74.
33. Sjöstedt A, Conlan JW, North RJ,. Neutrophils are critical for host defense against primary infection with the facultative intracellular bacterium Francisella tularensis in mice and participate in defense against reinfection. Infect Immun 1994; 62: 2779-83.
34. Liu JH, Wei S, Lamy T, et al,. Chronic neutropenia mediated by fas ligand. Blood 2000; 95: 3219-22.
35. Coacley G, Iqbal M, Brooks D, Panayi GS, Lanchbury JS,. CD8+ CD57+ T cells suppress neutrophil development in vitro: implications for the neutropenia of Felty's and large granular lymphocyte syndromes. Arthritis Rheum 2000; 43: 834-43.
36. Favalli EG, Varenna M, Sinigaglia L,. Drug-induced agranulocytosis during treatment with infliximab in enteropathic spondyloarthropathy. Clin Exp Rheumatol 2005; 23: 247-50.
37. Bathon JM, Martin RW, Fleischmann RM, et al,. A comparison of etanercept and methotrexate in patients with early rheumatoid arthritis. N Engl J Med 2000; 343: 1586-93.
38. Rajakulendran S, Gadsby K, Allen D, O'Reilly S, Deighton C,. Neutropenia while receiving anti-tumour necrosis factor treatment for rheumatoid arthritis. Ann Rheum Dis 2006; 65: 1678-9.
39. Theodoridou A, Kartsios C, Yiannaki E, Markala D, Settas L,. Reversible T-large granular lymphocyte expansion and neutropenia associated with adalimumab therapy. Rheumatol Int 2006; 27: 201-2.
40. Montané E, Sallés M, Barriocanal A, Riera E, Costa J, Tena X,. Antitumor necrosis factor-induced neutropenia: a case report with double positive rechallenges. Clin Rheumatol 2007; 26: 1527-9.
41. Wenham C, Gadsby K, Deighton C,. Three significant cases of neutropenia with etanercept. Rheumatology (Oxford) 2008; 47: 376-7.
42. Levälampi T, Korpela M, Vuolteenaho K, Moilanen E,. Etanercept and adalimumab treatment in patients with rheumatoid arthritis and spondyloarthropathies in clinical practice: adverse events and other reasons leading to discontinuation of the treatment. Rheumatol Int 2008; 28: 261-9.
43. Ottaviani S, Cerf-Payrastre I, Kemiche F, Pertuiset E,. Adalimumab-induced neutropenia in a patient with rheumatoid arthritis. Joint Bone Spine 2009; 76: 312-3.
44. Datta K, Ghosh RK, Ghosh SM,. Serious neutropenia following Etanercept administration in a 62 years female patient of rheumatoid arthritis. J Assoc Physicians India 2010; 58: 643-4.
45. Hastings R, Ding T, Butt S, et al,. Neutropenia in patients receiving anti-tumor necrosis factor therapy. Arthritis Care Res (Hoboken) 2010; 62: 764-9.
46. Sherlock ME, Bandsma R, Ota K, Kirby-Allen M, Griffiths AM,. Severe neutropenia following infliximab treatment in a child with ulcerative colitis. Inflamm Bowel Dis 2011; 17: E17-8.
47. Haroon M, Daly M, Harney S,. Re-challenge with Etanercept in patients with etanercept-induced Neutropenia. Clin Rheumatol 2012; 31: 151-5.
48. Benichou C, Solal-Celigny P,. Standardization of definitions and criteria for causality assessment of adverse drug reaction. Drug-induced blood cytopenias: report of an international consensus meeting. Nouvelle Revue Francaise d'Hematologie 1993; 33: 257-62.
49. British Society of Rheumatology on safety of anti-TNF therapies. Available at:. Accessed June 12, 2012.
50. Solem CA, Loftus EV, Tremaine WJ, Sandborn WJ,. Venous thromboembolism in inflammatory bowel disease. Am J Gastroenterol 2004; 99: 97-101.
51. Siegel SA, Shealy DJ,. The mouse/human chimeric monoclonal antibody cA2 neutralizes TNF in vitro and protects transgenic mice from cachexia and TNF lethality in vivo. Cytokine 1995; 7: 15-25.
52. Hommes DW, Van Dullemen HM,. Beneficial effect of treatment with a monoclonal anti-tumor necrosis factor-alpha antibody on markers of coagulation and fibrinolysis in patients with active Crohn's disease. Haemostasis 1997; 27: 269-77.
53. Van Oosten BW, Barkhof F, Truyen L, et al,. Increased MRI activity and immune activation in two multiple sclerosis patients treated with the monoclonal anti-tumor necrosis factor antibody cA2. Neurology. 1996; 47: 1531-4.
54. Ferraccioli G, Gremese E,. Thrombogenicity of TNF alpha in rheumatoid arthritis defined through biological probes: TNF alpha blockers. Autoimmun Rev 2004; 3: 261-6.
55. Jonsdottir T, Bratt J, Klareskog L, Van Vollenhoven R,. Development of ACLA (anti-cardiolipin antibodies) in patients treated with infliximab (remicade). Arthritis Rheum 2001; 44 (Suppl.): S373.
56. Korswagen LA, Bartelds GM, Krieckaert CL, et al,. Venous and arterial thromboembolic events in adalimumab-treated patients with antiadalimumab antibodies: a case series and cohort study. Arthritis Rheum 2011; 63: 877-83.
57. Popa C, Netea MG, van Riel PL, van der Meer JW, Stalenhoef AF,. The role of TNF-α in chronic inflammatory conditions, intermediary metabolism, and cardiovascular risk. J Lipid Res 2007; 48: 751-62.
58. Barnabe C, Martin BJ, Ghali WA,. Systematic review and meta-analysis: anti-tumor necrosis factor α therapy and cardiovascular events in rheumatoid arthritis. Arthritis Care Res (Hoboken) 2011; 63: 522-9.
59. Mortimore M, Gibson PR, Selby WS, Radford-Smith GL, Florin TH, Schering Plough (Australia). Early Australian experience with infliximab, a chimeric antibody against tumour necrosis factor-alpha, in the treatment of Crohn's disease: is its efficacy augmented by steroid-sparing immunosuppressive therapy? The Infliximab User Group. Intern Med J 2001; 31: 146-50.
60. Yee AM, Pochapin MB,. Treatment of complicated sarcoidosis with infliximab anti-tumor necrosis factor-alpha therapy. Ann Intern Med 2001; 135: 27-31.
61. Eklund KK, Peltomaa R, Leirisalo-Repo M,. Occurrence of pulmonary thromboembolism during infliximab therapy. Clin Exp Rheumatol 2003; 21: 679.
62. Puli SR, Benage DD,. Retinal vein thrombosis after infliximab (Remicade) treatment for Crohn's disease. Am J Gastroenterol 2003; 98: 939-40.
63. Ljung T, Karlén P, Schmidt D, et al,. Infliximab in inflammatory bowel disease: clinical outcome in a population based cohort from Stockholm County. Gut 2004; 53: 849-53.
64. Ryan BM, Romberg M, Wolters F, Stockbrugger RW,. Extensive forearm deep venous thrombosis following a severe infliximab infusion reaction. Eur J Gastroenterol Hepatol 2004; 16: 941-2.
65. Sobkeng Goufack E, Mammou S, Scotto B, et al,. Paroxysmal nocturnal hemoglobinuria revealed by hepatic vein thrombosis (Budd-Chiari syndrome) during Infliximab therapy. Gastroenterol Clin Biol 2004; 28: 596-9.
66. Grange L, Nissen MJ, Garambois K, et al,. Infliximab-induced cerebral thrombophlebitis. Rheumatology (Oxford) 2005; 44: 260-1.
67. Nosbaum A, Goujon C, Fleury B, Guillot I, Nicolas JF, Bérard F,. Arterial thrombosis with anti-phospholipid antibodies induced by infliximab. Eur J Dermatol 2007; 17: 546-7.
68. Veerappan SG, Kennedy M, O'Morain CA, Ryan BM,. Retinal vein thrombosis following infliximab treatment for severe left-sided ulcerative colitis. Eur J Gastroenterol Hepatol 2008; 20: 588-9.
69. Aringer M, Houssiau F, Gordon C, et al,. Adverse events and efficacy of TNF-alpha blockade with infliximab in patients with systemic lupus erythematosus: long-term follow-up of 13 patients. Rheumatology (Oxford) 2009; 48: 1451-4.
70. Petitpain N, Gambier N, Wahl D, Chary-Valckenaere I, Loeuille D, Gillet P, French Network of Pharmacovigilance Centers. Arterial and venous thromboembolic events during anti-TNF therapy: a study of 85 spontaneous reports in the period 2000-2006. Biomed Mater Eng 2009; 19: 355-64.
71. Vergou T, Moustou AE, Maniateas A, Stratigos AJ, Katsambas A, Antoniou C,. Central retinal vein occlusion following infliximab treatment for plaque-type psoriasis. Int J Dermatol 2010; 49: 1215-7.
72. Makol A, Grover M, Guggenheim C, Hassouna H,. Etanercept and venous thromboembolism: a case series. J Med Case Reports 2010; 4: 12.
73. Mehta Shameer J, Berger J, Tang Kwok H,. Peripheral arterial thrombosis following administration of infliximab for Crohn disease. Grand Rounds 2010; 10: 78-81.
74. Diniz B, Barbosa CP, Regatieri CV, Rodrigues EB,. Branch retinal vein occlusion following infliximab treatment: case report. Arq Bras Oftalmol 2011; 74: 214-6.
75. Cognat E, Crassard I, Denier C, Vahedi K, Bousser MG,. Cerebral venous thrombosis in inflammatory bowel diseases: eight cases and literature review. Int J Stroke 2011; 6: 487-92.
76. Leblanc S, Lloret Linares C, Cacheux W, Mouthon L, Chaussade S,. Aortic thrombosis in young women with Crohn's disease receiving adalimumab: report of two cases. Inflamm Bowel Dis 2011; 17: 862-3.
77. Quartier P, Taupin P, Bourdeaut F, et al,. Efficacy of etanercept for the treatment of juvenile idiopathic arthritis according to the onset type. Arthritis Rheum 2003; 48: 1093-101.
78. Szalay B, Acs L, Vásárhelyi B, Kovács L, Balog A,. Successful use of tocilizumab in a patient with rheumatoid arthritis following severe pancytopenia during etanercept therapy. J Clin Rheumatol 2011; 17: 377-9.
79. Kuruvilla J, Leitch HA, Vickars LM, et al,. Aplastic anemia following administration of a tumor necrosis factor-alpha inhibitor. Eur J Haematol 2003; 71: 396-8.
80. Seiderer J, Göke B, Ochsenkühn 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.
81. Menon Y, Cucurull E, Espinoza LR,. Pancytopenia in a patient with scleroderma treated with infliximab. Rheumatology (Oxford) 2003; 42: 1273-4.
82. Marchesoni A, Arreghini M, Panni B, Battafarano N, Uziel L,. Life-threatening reversible bone marrow toxicity in a rheumatoid arthritis patient switched from leflunomide to infliximab. Rheumatology (Oxford) 2003; 42: 193-4.
83. Ben Salem C, et al,. Infliximab-induced bone marrow aplasis and vasculitis, 9th Annual Meeting of the International Society of Pharmacovigilance, Abstr. 10, Reims, France, 6 October 2009.
84. Metyas SK, Tadros RM, Arkfeld DG,. Adalimumab-induced noncaseating granuloma in the bone marrow of a patient being treated for rheumatoid arthritis. Rheumatol Int 2009; 29: 437-9.
85. Tyler LN, Harville TO, Blackall DP,. Multiple alloantibodies after transfusion in an infant treated with infliximab. N Engl J Med 2007; 357: 2092-3.
86. Vermeire S, Noman M, Van Assche G, et al,. Autoimmunity associated with anti-tumor necrosis factor alpha treatment in Crohn's disease: a prospective cohort study. Gastroenterology 2003; 125: 32-9.
87. Chauveau E, Terrier F, Casassus-Buihle D, Moncoucy X, Oddes B,. Macrophage activation syndrome after treatment with infliximab for fistulated Crohn's disease. Presse Med 2005; 34: 583-4.
88. Ramanan AV, Schneider R,. Macrophage activation syndrome following initiation of etanercept in a child with systemic onset juvenile rheumatoid arthritis. J Rheumatol 2003; 30: 401-3.
89. Moltõ A, Mateo L, Lloveras N, Olivé A, Minguez S,. Visceral leishmaniasis and macrophagic activation syndrome in a patient with rheumatoid arthritis under treatment with adalimumab. Joint Bone Spine 2010; 77: 271-3.
90. Cancelliere N, Barranco P, Vidaurrázaga C, Benito DM, Quirce S,. Subacute prurigo and eosinophilia in a patient with rheumatoid arthritis receiving infliximab and etanercept. J Investig Allergol Clin Immunol 2011; 21: 248-9.
91. Rubin DT, Sohi S, Shilling R, White S,. Pulmonary eosinophilia associated with infliximab treatment of Crohn's disease. Ame J Gastroenterol 2005; 100 (Suppl. S): S224-5.
92. Tugnet N, Youssef A, Whallett AJ,. Wells' syndrome (eosinophilic cellulitis) secondary to infliximab. Rheumatology (Oxford) 2012; 51: 195-6.
93. Poliak N, Orange JS, Pawel BR, Weiss PF,. Eosinophilic fasciitis mimicking angioedema and treatment response to infliximab in a pediatric patient. Ann Allergy Asthma Immunol 2011; 106: 444-5.
94. Vestergaard C, Deleuran M, Kragballe K,. Two cases of atopic dermatitis-like conditions induced in psoriasis patients treated with infliximab. J Eur Acad Dermatol Venereol 2007; 21: 1272-4.