Current and future treatments for Behçet's uveitis: Road to remission

International Ophthalmology

Volumn 34, Issue 2, 2014, Pages 365-381

  Mesquida, Marina ^a   Molins, Blanca ^b   Llorenç, Victor ^a   Hernández, María Victoria ^a   Espinosa, Gerard ^a   Dick, Andrew D ^c   Adán, Alfredo ^a  

^a UNIVERSITY OF BARCELONA   (Spain)

^b INSTITUT D INVESTIGACIONS BIOMÈDIQUES AUGUST PI I SUNYER IDIBAPS   (Spain)

^c UNIVERSITY OF BRISTOL   (United Kingdom)

Author keywords

Beh et's disease; Biological drugs; IFN ; IL 1; IL 6; TNF ; Uveitis

Indexed keywords

ABATACEPT; ADALIMUMAB; ALPHA INTERFERON; AZATHIOPRINE; CALCINEURIN INHIBITOR; CANAKINUMAB; CERTOLIZUMAB PEGOL; CORTICOSTEROID; ETANERCEPT; GEVOKIZUMAB; GOLIMUMAB; IMMUNOSUPPRESSIVE AGENT; INFLIXIMAB; INTERLEUKIN 1 RECEPTOR BLOCKING AGENT; RECOMBINANT INTERLEUKIN 1 RECEPTOR BLOCKING AGENT; RITUXIMAB; TACROLIMUS; TOCILIZUMAB; TUMOR NECROSIS FACTOR ALPHA INHIBITOR;

AUTOIMMUNE UVEITIS; BEHCET DISEASE; BEHCET UVEITIS; ENVIRONMENTAL FACTOR; HEREDITY; HUMAN; PHASE 3 CLINICAL TRIAL (TOPIC); RANDOMIZED CONTROLLED TRIAL (TOPIC); REMISSION; REVIEW;

ADRENAL CORTEX HORMONES; BEHCET SYNDROME; BIOLOGICAL FACTORS; HUMANS; IMMUNOSUPPRESSIVE AGENTS; INTERFERONS; UVEITIS;

EID: 84898847548     PISSN: 01655701     EISSN: 15732630     Source Type: Journal    
DOI: 10.1007/s10792-013-9788-5     Document Type: Review

References (105)

1. Deuter CM, Kötter I, Wallace GR, Murray PI, Stübiger N, Zierhut M (2008) Behçet's disease: ocular effects and treatment. Prog Retin Eye Res 27:111-136
2. Behçet H (1937) Überrezidivierendeaphthösedurchein Virus verursachte Geschwüre am Mund, am Auge und an den Genitalien. Dermatol Wochenschr 105:1152-1157
3. International Study Group for Behçet's Disease (1990) Criteria for diagnosis of Behçet's disease. Lancet 335:1078-1080
4. Khairallah M, Accorinti M, Muccioli C, Kahloun R, Kempen JH (2012) Epidemiology of Behçet disease. Ocul Immunol Inflamm 20:324-335
5. Azizerli G, Kose AA, Sarica R et al (2003) Prevalence of Behçet's disease in Istanbul, Turkey. Int J Dermatol 42:803-806
6. Kapsimali VD, Kanakis MA, Vaiopoulos GA, Kaklamanis PG (2010) Etiopathogenesis of Behçet's disease with emphasis on the role of immunological aberrations. Clin Rheumatol 29:1211-1216
7. Mendoza-Pinto C, García-Carrasco M, Jiménez- Hernández M et al (2010) Etiopathogenesis of Behcet's disease. Autoimmun Rev 9:241-245
8. Maldini C, Lavalley MP, Cheminant M, de Menthon M, Mahr A (2012) Relationships of HLA-B51 or B5 genotype with Behcet's disease clinical characteristics: systematic review and meta-analyses of observational studies. Rheumatology (Oxf) 51:887-900
9. Hazirolan D, Stübiger N, Pleyer U (2012) Light on the Horizont: biologicals in Behçet uveitis. Acta Ophthalmol. doi: 10.1111/j.1755-3768. 2011.02348.x
10. Zhou ZY, Chen SL, Shen N, Lu Y (2012) Cytokines and Behcet's disease. Autoimmun Rev 11:699-704
11. Hamzaoui K, Hamzaoui A, Guemira F et al (2002) Cytokine profile in Behçet's disease patients. Relationship with disease activity. Scand J Rheumatol 31:205-210
12. Mochizuki M, Akduman L, Nussenblatt RB (1996) Behçet's disease. In: Pepose JS, Holland GN, Wilhelmus KR (eds) Ocular infection and immunity. Mosby, St. Louis, pp 663-675
13. Davatchi F, Shahram F, Chams-Davatchi C et al (2010) Behçet's disease: from East to West. Clin Rheumatol 29:823-833
14. Tugal-Tutkun I, Onal S, Altan-Yaycioglu R, Huseyin Altunbas H, Urgancioglu M (2004) Uveitis in Behçet disease: an analysis of 880 patients. Am J Ophthalmol 138:373-380
15. Yang P, Fang W, Meng Q et al (2008) Clinical features of Chinese patients with Behçet's disease. Ophthalmology 115:312-318
16. Kitaichi N, Miyazaki A, Stanford MR et al (2007) Ocular features of Behçet's disease: an international collaborative study. Br J Ophthalmol 91:1579-1582
17. Saleh OA, Birnbaum AD, Tessler HH et al (2012) Behçet uveitis in the American Midwest. Ocul Immunol Inflamm 20:12-17
18. Markomichelakis N, Delicha E, Masselos S et al (2011) A single infliximab infusion vs corticosteroids for acute panuveitis attacks in Behçet's disease: a comparative 4-week study. Rheumatology (Oxf) 50:593-597
19. Rhen T, Cidlowski JA (2005) Antiinflammatory action of glucocorticoids - new mechanisms for old drugs. N Engl J Med 353:1711-1723
20. Tanaka T, Suzuki J, Yamakawa N, Usui M (2000) Steroid sensitivity and postoperative course of seven patients with Behçet's disease. Ophthalmic Res 32:41-43
21. Taylor SR, Singh J, Menezo V et al (2011) Behçet disease: visual prognosis and factors influencing the development of visual loss. Am J Ophthalmol 152:1059-1066
22. Binder AI, Graham EM, Sanders MD, Dinning W, James DG, Denman AM (1987) Cyclosporin A in the treatment of severe Behcet's uveitis. Br J Rheumatol 26:285-291
23. BenEzra D, Cohen E, Chajek T et al (1988) Evaluation of conventional therapy versus cyclosporine A in Behçet's syndrome. Transplant Proc 20:136-143
24. Ozyazgan Y, Yurdakul S, Yazici H et al (1992) Low dose cyclosporin A versus pulsed cyclophosphamide in Behcet's syndrome: a single masked trial. Br J Ophthalmol 76:241-243
25. Kotake S, Higashi K, Yoshikawa K et al (1999) Central nervous system symptoms in patients with Behcet disease receiving cyclosporine therapy. Ophthalmology 106:586-589
26. Yazici H, Yurdakul S, Hamuryudan V (2001) Behcet disease. Curr Opin Rheumatol 13:18-22
27. Kilmartin DJ, Forrester JV, Dick AD (1998) Tacrolimus (FK506) in failed cyclosporin A therapy in endogenous posterior uveitis. Ocul Immunol Inflamm 6:101-109
28. Murphy CC, Greiner K, Plskova J et al (2005) Cyclosporine vs tacrolimus therapy for posterior and intermediate uveitis. Arch Ophthalmol 123:634-641
29. Tanabe K (2003) Calcineurin inhibitors in renal transplantation: what is the best option? Drugs 63:1535-1548
30. Yazici H, Pazarli H, Barnes CG et al (1990) A controlled trial of azathioprine in Behcet's syndrome. N Engl J Med 322:281-285
31. Saadoun D, Wechsler B, Terrada C et al (2010) Azathioprine in severe uveitis of Behçet's disease. Arthritis Care Res (Hoboken) 62:1733-1738
32. Hatemi G, Silman A, Bang D et al (2009) Management of Behçet disease: a systematic literature review for the European League Against Rheumatism evidence-based recommendations for the management of Behçet disease. Ann Rheum Dis 68:1528-1534
33. Kaburaki T, Araki F, Takamoto M et al (2010) Best-corrected visual acuity and frequency of ocular attacks during the initial 10 years in patients with Behçet's disease. Graefes Arch Clin Exp Ophthalmol 248:709-714
34. Sharma SM, Nestel AR, Lee RW, Dick AD (2009) Clinical review: anti-TNFalpha therapies in uveitis: perspective on 5 years of clinical experience. Ocul Immunol Inflamm 17(6):403-414
35. Theofilopoulos AN, Baccala R, Beutler B, Kono DH (2005) Type I interferons (alpha/-beta) in immunity and autoimmunity. Annu Rev Immunol 23:307-336
36. Treusch M, Vonthein R, Baur M et al (2004) Influence of human recombinant interferon-alpha2a (rhIFN-alpha2a) on altered lymphocyte subpopulations and monocytes in Behcet's disease. Rheumatology (Oxf) 43:1275-1282
37. Yang DS, Talylor SR, Lightman SL (2008) Interferon-alpha in the management of patients with Behçet's disease. Br J Hosp Med (Lond) 69:575-579
38. Zouboulis CC, Orfanos CE (1998) Treatment of Adamantiades-Behcet disease with systemic interferon alfa. Arch Dermatol 134:1010-1016
39. Alpsoy E, Durusoy C, Yilmaz E et al (2002) Interferon alfa-2a in the treatment of Behcet disease: a randomized placebo-controlled and double-blind study. Arch Dermatol 138:467-471
40. Warde N (2010) Therapy: Behçet uveitis: good results for IFN-alpha-2a. Nat Rev Rheumatol 6:437
41. Deuter CM, Zierhut M, Möhle A et al (2010) Long-term remission after cessation of interferon-α treatment in patients with severe uveitis due to Behçet's disease. Arthritis Rheum 62:2796-2805
42. Kötter I, Günaydin I, Zierhut M, Stübiger N (2004) The use of interferon a in Behcet disease: review of the literature. Semin Arthritis Rheum 33:320-335
43. Stübiger N, Kötter I, Zierhut M (2000) Complete regression of retinal neovascularisation after therapy with interferon alfa in Behcet's disease. Br J Ophthalmol 84:1437-1438
44. Dick AD, Forrester JV, Liversidge J et al (2004) The role of tumour necrosis factor (TNF-alpha) in experimental autoimmune uveoretinitis (EAU). Prog Retin Eye Res 23:617-637
45. El-Asrar AM, Struyf S, Kangave D et al (2011) Cytokine profiles in aqueous humor of patients with different clinical entities of endogenous uveitis. Clin Immunol 139:177-184
46. Ahn JK, Yu HG, Chung H, Park YG (2006) Intraocular cytokine environment in active Behçet uveitis. Am J Ophthalmol 142:429-434
47. Dick AD, McMenamin PG, Körner H, Scallon BJ, Ghrayeb J, Forrester JV et al (1996) Inhibition of tumor necrosis factor activity minimizes target organ damage in experimental autoimmune uveoretinitis despite quantitatively normal activated T cell traffic to the retina. Eur J Immunol 26:1018-1025
48. Murphy CC, Greiner K, Plskova J, Duncan L, Frost A, Isaacs JD et al (2004) Neutralizing tumor necrosis factor activity leads to remission in patients with refractory noninfectious posterior uveitis. Arch Ophthalmol 122:845-851
49. Arida A, Fragiadaki K, Giavri E, Sfikakis PP (2011) Anti-TNF agents for Behçet's disease: analysis of published data on 369 patients. Semin Arthritis Rheum 41(1):61-70
50. Sfikakis PP, Kaklamanis PH, Elezoglou A et al (2004) Infliximab for recurrent, sight-threatening ocular inflammation in Adamantiades-Behcet disease. Ann Intern Med 140:404-406
51. Ohno S, Nakamura S, Hori S et al (2004) Efficacy, safety, and pharmacokinetics of multiple administration of infliximab in Behcet's disease with refractory uveoretinitis. J Rheumatol 31:1362-1368
52. Yamada Y, Sugita S, Tanaka H et al (2010) Comparison of infliximab versus cyclosporin during the initial 6-month treatment period in Behçet disease. Br J Ophthalmol 94:284-288
53. Tugal-Tutkun I, Mudun A, Urgancioglu M et al (2005) Efficacy of infliximab in the treatment of uveitis that is refractory to treatment with the combination of azathioprine, cyclosporine, and corticosteroids in Behçet's disease. An open-label trial. Arthritis Rheum 52:2478-2484
54. Okada AA, Goto H, Ohno S, Mochizuki M, Ocular Behçet's Disease Research Group Of Japan (2012) Multicenter study of infliximab for refractory uveoretinitis in Behçet disease. Arch Ophthalmol 130(5):592-598
55. Bawazeer A, Raffa LH, Nizamuddin SH (2010) Clinical experience with adalimumab in the treatment of ocular Behçet disease. Ocul Immunol Inflamm 18:226-232
56. Díaz-Llopis M, Salom D, Garcia-de-Vicuña C, Cordero-Coma M, Ortega G, Ortego N et al (2012) Treatment of refractory uveitis with adalimumab: a prospective multicenter study of 131 patients. Ophthalmology 119:1575-1581
57. Perra D, Alba MA, Callejas JL, Mesquida M, Ríos-Fernández R, Adán A et al (2012) Adalimumab for the treatment of Behcet's disease: experience in 19 patients. Rheumatology (Oxf) 51:1825-1831
58. Takase K, Ohno S, Ideguchi H, Uchio E, Takeno M, Ishigatsubo Y (2011) Successful switching to adalimumab in an infliximab-allergic patient with severe Behçet disease-related uveitis. Rheumatol Int 31:243-245
59. Leccese P, Latanza L, D'Angelo S, Padula A, Olivieri I (2011) Efficacy of switching to adalimumab in a patient with refractory uveitis of Behçet's disease to infliximab. Clin Exp Rheumatol 29(4 Suppl 67):S93
60. Cordero-Coma M, Salom D, Díaz-Llopis M, López-Prats MJ, Calleja S (2011) Golimumab for uveitis. Ophthalmology 118:1892.e3-1892.e4
61. William M, Faez S, Papaliodis GN, Lobo AM (2012) Golimumab for the treatment of refractory juvenile idiopathic arthritis-associated uveitis. J Ophthalmic Inflamm Infect 2(4):231-233
62. Mesquida M, Hernández MV, Llorenç V, Pelegrín L, Espinosa G, Dick AD, et al (2012) Behçet disease-associated uveitis successfully treated with golimumab. Ocul Immunol Inflamm 21(2):160-162
63. Galor A, Perez VL, Hammel JP, Lowder CY (2006) Differential effectiveness of etanercept and infliximab in the treatment of ocular inflammation. Ophthalmology 113:2137-2323
64. Sfikakis PP, Markomichelakis N, Alpsoy E et al (2007) Anti-TNF therapy in the management of Behçet's disease - review and basis for recommendations. Rheumatology (Oxf) 46:736-741
65. Suhler EB, Smith JR, Wertheim MS et al (2005) A prospective trial of infliximab therapy for refractory uveitis: preliminary safety and efficacy outcomes. Arch Ophthalmol 123(7):903-912
66. Niccoli L, Nannini C, Benucci M et al (2007) Long-term efficacy of infliximab in refractory posterior uveitis of Behçet's disease: a 24-month follow-up study. Rheumatology (Oxf) 46(7):1161-1164
67. Adán A, Hernandez V, Ortiz S, Molina JJ, Pelegrin L, Espinosa G, Sanmartí R (2010) Effects of infliximab in the treatment of refractory posterior uveitis of Behçet's disease after withdrawal of infusions. Int Ophthalmol 30(5):577-581
68. Sugita S, Yamada Y, Kaneko S, Horie S, Mochizuki M (2011) Induction of regulatory T cells by infliximab in Behcet's disease. Investig Ophthalmol Vis Sci 52:476-484
69. Bodaghi B, Gendron G, Wechsler B et al (2007) Efficacy of interferon alpha in the treatment of refractory and sight threatening uveitis: a retrospective monocentric study of 45 patients. Br J Ophthalmol 91:335-339
70. Kotter I, Deuter C, Stubiger N, Zierhut M (2005) Interferon-a (IFN-a) application versus tumor necrosis factor-a antagonism for ocular Behçet's disease: focusing more on IFN. J Rheumatol 32(8):1633 (author reply 1634)
71. Nestorov I (2005) Clinical pharmacokinetics of TNF antagonists: How do they differ? Semin Arthritis Rheum 34(5 Suppl 1):12-18
72. Mushtaq B, Saeed T, Situnayake RD, Murray PI (2007) Adalimumab for sight-threatening uveitis in Behçet's disease. Eye (Lond) 21(6):824-825
73. Bawazeer A, Raffa LH, Nizamuddin SH (2010) Clinical experience with adalimumab in the treatment of ocular Behçet disease. Ocul Immunol Inflamm 18(3):226-232
74. Perra D, Alba MA, Callejas JL, Mesquida M, Ríos-Fernández R, Adán A, Ortego N, Cervera R, Espinosa G (2012) Adalimumab for the treatment of Behcet's disease: experience in 19 patients. Rheumatology (Oxf) 51(10):1825-1831
75. Olivieri I, Leccese P, D'Angelo S, Padula A, Nigro A, Palazzi C, Coniglio G, Latanza L (2011) Efficacy of adalimumab in patients with Behçet's disease unsuccessfully treated with infliximab. Clin Exp Rheumatol 29(4 Suppl 67):S54-S57
76. Takase K, Ohno S, Ideguchi H, Uchio E, Takeno M, Ishigatsubo Y (2011) Successful switching to adalimumab in an infliximab-allergic patient with severe Behçet disease-related uveitis. Rheumatol Int 31(2):243-245
77. Keystone E, Genovese MC, Klareskog L et al (2010) Golimumab in patients with active rheumatoid arthritis despite methotrexate therapy: 52-week results of the GO-FORWARD study. Ann Rheum Dis 69:1129-1135
78. Smolen JS, Kay J, Landewé RB et al (2012) Golimumab in patients with active rheumatoid arthritis who have previous experience with tumour necrosis factor inhibitors: results of a long-term extension of the randomised, double-blind, placebo-controlled GO-AFTER study through week 160. Ann Rheum Dis 71(10):1671-1679
79. Keystone E, Genovese MC, Klareskog L, Hsia EC, Hall S, Miranda PC, Pazdur J, Bae SC, Palmer W, Xu S, Rahman MU (2010) Golimumab in patients with active rheumatoid arthritis despite methotrexate therapy: 52-week results of the GO-FORWARD study. Ann Rheum Dis 69(6):1129-1135
80. Maini R, St Clair EW, Breedveld F, Furst D, Kalden J, Weisman M, Smolen J, Emery P, Harriman G (1999) Infliximab (chimeric anti-tumour necrosis factor alpha monoclonal antibody) versus placebo in rheumatoid arthritis patients receiving concomitant methotrexate: a randomised phase III trial. ATTRACT Study Group. Lancet 354(9194):1932-1939
81. Dinarello CA, Simon A, van der Meer JW (2012) Treating inflammation by blocking interleukin-1 in a broad spectrum of diseases. Nat Rev Drug Discov 11(8):633-652
82. Gül A (2005) Behçet's disease as an autoinflammatory disorder. Curr Drug Targets Inflamm Allergy 4:81-83
83. Mege JL, Dilsen N, Sanguedolce V et al (1993) Overproduction of monocyte derived tumor necrosis factor alpha, interleukin (IL) 6, IL-8 and increased neutrophil superoxide generation in Behçet's disease. A comparative study with familial Mediterranean fever and healthy subjects. J Rheumatol 20(9):1544-1549
84. Teoh SC, Sharma S, Hogan A et al (2007) Tailoring biological treatment: anakinra treatment of posterior uveitis associated with the CINCA syndrome. Br J Ophthalmol 91:263-264
85. Botsios C, Sfriso P, Furlan A, Punzi L, Dinarello CA (2008) Resistant Behçet disease responsive to anakinra. Ann Intern Med 149(4):284-286
86. Düzgün N, Ayaşlioǧlu E, Tutkak H, Aydintuǧ OT (2005) Cytokine inhibitors: soluble tumor necrosis factor receptor 1 and interleukin-1 receptor antagonist in Behçet's disease. Rheumatol Int 25(1):1-5
87. Blech M, Peter D, Fischer P (2012) One target-two different binding modes: structural insights into gevokizumab and canakinumab interactions to interleukin-1β. J Mol Biol (in press)
88. Church LD, McDermott MF (2009) Canakinumab, a fully-human mAb against IL-1beta for the potential treatment of inflammatory disorders. Curr Opin Mol Ther 11:81-89
89. Cantarini L, Vitale A, Borri M, Galeazzi M, Franceschini R (2012) Successful use of canakinumab in a patient with resistant Behçet's disease. Clin Exp Rheumatol 30(3 Suppl 72):S115
90. Ugurlu S, Ucar D, Seyahi E, Hatemi G, Yurdakul S (2012) Canakinumab in a patient with juvenile Behçet's syndrome with refractory eye disease. Ann Rheum Dis 71:1591-1592
91. Geiler J, McDermott MF (2010) Gevokizumab, an anti-IL-1β mAb for the potential treatment of type 1 and 2 diabetes, rheumatoid arthritis and cardiovascular disease. Curr Opin Mol Ther 12:755-769
92. Gül A, Tugal-Tutkun I, Dinarello CA, Reznikov L, Esen BA, Mirza A, Scannon P, Solinger A (2012) Interleukin-1β-regulating antibody XOMA 052 (gevokizumab) in the treatment of acute exacerbations of resistant uveitis of Behcet's disease: an open-label pilot study. Ann Rheum Dis 71(4):563-566
93. Hirano T, Yasukawa K, Harada H et al (1986) Complementary DNA for a novel human interleukin (BSF-2) that induces B lymphocytes to produce immunoglobulin. Nature 324(6092):73-76
94. Kaly L, Rosner I (2012) Tocilizumab - a novel therapy for non-organ-specific autoimmune diseases. Best Pract Res Clin Rheumatol 26:157-165
95. Kimura A, Kishimoto T (2010) IL-6: regulator of Treg/Th17 balance. Eur J Immunol 40(7):1830-1835
96. Geri G, Terrier B, Rosenzwajg M et al (2011) Critical role of IL-21 in modulating TH17 and regulatory T cells in Behçet disease. J Allergy Clin Immunol 128(3):655-664
97. Ogata A, Tanaka T (2012) Tocilizumab for the treatment of rheumatoid arthritis and other systemic autoimmune diseases: current perspectives and future directions. Int J Rheumatol. doi: 10.1155/2012/946048
98. Hirano T, Ohguro N, Hohki S et al (2012) A case of Behçet's disease treated with a humanized anti-interleukin-6 receptor antibody, tocilizumab. Mod Rheumatol 22:298-302
99. Miserocchi E, Pontikaki I, Modorati G, Gattinara M, Meroni PL, Gerloni V (2011) Anti-CD 20 monoclonal antibody (rituximab) treatment for inflammatory ocular diseases. Autoimmun Rev 11(1):35-39
100. Miserocchi E, Pontikaki I, Modorati G, Bandello F, Meroni PL, Gerloni V (2011) Rituximab for uveitis. Ophthalmology 118(1):223-224
101. Heiligenhaus A, Miserocchi E, Heinz C, Gerloni V, Kotaniemi K (2011) Treatment of severe uveitis associated with juvenile idiopathic arthritis with anti-CD20 monoclonal antibody (rituximab). Rheumatology (Oxf) 50(8):1390-1394
102. Davatchi F, Shams H, Rezaipoor M et al (2010) Rituximab in intractable ocular lesions of Behcet's disease; randomized single-blind control study (pilot study). Int J Rheum Dis 13:246-252
103. Sadreddini S, Noshad H, Molaeefard M, Noshad R (2008) Treatment of retinal vasculitis in Behçet's disease with rituximab. Mod Rheumatol 18:306-308
104. Lee RW, Dick AD (2010) Treat early and embrace the evidence in favour of anti-TNF-alpha therapy for Behçet's uveitis. Br J Ophthalmol 94(3):269-270
105. Benitah NR, Sobrin L, Papaliodis GN (2011) The use of biologic agents in the treatment of ocular manifestations of Behcet's disease. Semin Ophthalmol 26:295-303