Skip to main content
Top
Published in: Clinical Rheumatology 2/2020

01-02-2020 | Uveitis | Review Article

Treating juvenile idiopathic arthritis (JIA)-related uveitis beyond TNF-α inhibition: a narrative review

Authors: Carla Gaggiano, Donato Rigante, Gian Marco Tosi, Antonio Vitale, Bruno Frediani, Salvatore Grosso, Claudia Fabiani, Luca Cantarini

Published in: Clinical Rheumatology | Issue 2/2020

Login to get access

Abstract

Chronic anterior uveitis is the most frequent among extra-articular manifestations of juvenile idiopathic arthritis (JIA) and a relevant cause of ocular morbidity in children. Asymmetric arthritis, early onset disease, female sex, and anti-nuclear antibody (ANA) positivity are counted among risk factors for developing this complication. It usually has insidious onset and asymptomatic chronic-relapsing course, but the persistence of low-grade chronic inflammation can lead to irreversible structural ocular damage and to vision-threatening complications. For such reasons, achieving a complete absence of inflammation through early targeted and aggressive treatments is a primary therapeutic goal in these patients. This review is aimed at summarizing scientific evidence about biologic rescue therapy of JIA-related uveitis in patients who fail to achieve clinical remission, in spite of being treated with conventional disease-modifying anti-rheumatic drugs (cDMARDs) and at least one biologic tumor necrosis factor (TNF)-α inhibitor. Interleukin (IL)-6 inhibition appears a promising and safe option for refractory JIA-related uveitis. Abatacept and rituximab proved to be beneficial as well, but their efficacy together with some safety concerns needs to be more extensively evaluated.
Literature
1.
go back to reference Saurenmann RK, Levin AV, Feldman BM, Rose JB, Laxer RM, Schneider R, Silverman ED (2007) Prevalence, risk factors, and outcome of uveitis in juvenile idiopathic arthritis: a long-term follow-up study. Arthritis Rheum 56:647–657PubMed Saurenmann RK, Levin AV, Feldman BM, Rose JB, Laxer RM, Schneider R, Silverman ED (2007) Prevalence, risk factors, and outcome of uveitis in juvenile idiopathic arthritis: a long-term follow-up study. Arthritis Rheum 56:647–657PubMed
2.
go back to reference Heiligenhaus A, Heinz C, Edelsten C, Kotaniemi K, Minden K (2013) Review for disease of the year: epidemiology of juvenile idiopathic arthritis and its associated uveitis: the probable risk factors. Ocul Immunol Inflamm 21:180–191PubMed Heiligenhaus A, Heinz C, Edelsten C, Kotaniemi K, Minden K (2013) Review for disease of the year: epidemiology of juvenile idiopathic arthritis and its associated uveitis: the probable risk factors. Ocul Immunol Inflamm 21:180–191PubMed
3.
go back to reference Martini A (2003) Are the number of joints involved or the presence of psoriasis still useful tools to identify homogeneous disease entities in juvenile idiopathic arthritis? J Rheumatol 30:1900–1903PubMed Martini A (2003) Are the number of joints involved or the presence of psoriasis still useful tools to identify homogeneous disease entities in juvenile idiopathic arthritis? J Rheumatol 30:1900–1903PubMed
4.
go back to reference Sen ES, Ramanan AV (2017) Juvenile idiopathic arthritis-associated uveitis. Best Pract Res Clin Rheumatol 31:517–534PubMed Sen ES, Ramanan AV (2017) Juvenile idiopathic arthritis-associated uveitis. Best Pract Res Clin Rheumatol 31:517–534PubMed
5.
go back to reference Clarke SL, Sen ES, Ramanan AV (2016) Juvenile idiopathic arthritis-associated uveitis. Pediatr Rheumatol Online J 14:27PubMedPubMedCentral Clarke SL, Sen ES, Ramanan AV (2016) Juvenile idiopathic arthritis-associated uveitis. Pediatr Rheumatol Online J 14:27PubMedPubMedCentral
6.
go back to reference Paroli MP, Spinucci G, Fabiani C, Pivetti-Pezzi P (2010) Retinal complications of juvenile idiopathic arthritis-related uveitis: a microperimetry and optical coherence tomography study. Ocul Immunol Inflamm 18:54–59PubMed Paroli MP, Spinucci G, Fabiani C, Pivetti-Pezzi P (2010) Retinal complications of juvenile idiopathic arthritis-related uveitis: a microperimetry and optical coherence tomography study. Ocul Immunol Inflamm 18:54–59PubMed
7.
go back to reference Paroli MP, Fabiani C, Spinucci G, Abicca I, Sapia A, Spadea L (2013) Severe macular edema in patients with juvenile idiopathic arthritis-related uveitis. Case Rep Ophthalmol Med 2013:803989PubMedPubMedCentral Paroli MP, Fabiani C, Spinucci G, Abicca I, Sapia A, Spadea L (2013) Severe macular edema in patients with juvenile idiopathic arthritis-related uveitis. Case Rep Ophthalmol Med 2013:803989PubMedPubMedCentral
8.
go back to reference Gregory AC, Kempen JH, Daniel E, Kaçmaz RO, Foster CS, Jabs DA, Levy-Clarke GA, Nussenblatt RB, Rosenbaum JT, Suhler EB, Thorne JE, Systemic Immunosuppressive Therapy for Eye Diseases Cohort Study Research Group (2013) Risk factors for loss of visual acuity among patients with uveitis associated with juvenile idiopathic arthritis: the systemic immunosuppressive therapy for eye diseases study. Ophthalmology 120:186–192PubMed Gregory AC, Kempen JH, Daniel E, Kaçmaz RO, Foster CS, Jabs DA, Levy-Clarke GA, Nussenblatt RB, Rosenbaum JT, Suhler EB, Thorne JE, Systemic Immunosuppressive Therapy for Eye Diseases Cohort Study Research Group (2013) Risk factors for loss of visual acuity among patients with uveitis associated with juvenile idiopathic arthritis: the systemic immunosuppressive therapy for eye diseases study. Ophthalmology 120:186–192PubMed
9.
go back to reference Bou R, Adán A, Borrás F, Bravo B, Calvo I, De Inocencio J, Díaz J, Escudero J, Fonollosa A, de Vicuña CG, Hernández V, Merino R, Peralta J, Rúa MJ, Tejada P, Antón J (2015) Clinical management algorithm of uveitis associated with juvenile idiopathic arthritis: interdisciplinary panel consensus. Rheumatol Int 35:777–785PubMed Bou R, Adán A, Borrás F, Bravo B, Calvo I, De Inocencio J, Díaz J, Escudero J, Fonollosa A, de Vicuña CG, Hernández V, Merino R, Peralta J, Rúa MJ, Tejada P, Antón J (2015) Clinical management algorithm of uveitis associated with juvenile idiopathic arthritis: interdisciplinary panel consensus. Rheumatol Int 35:777–785PubMed
10.
go back to reference Perez VL, Papaliodis GN, Chu D, Anzaar F, Christen W, Foster CS (2004) Elevated levels of interleukin 6 in the vitreous fluid of patients with pars planitis and posterior uveitis: the Massachusetts eye & ear experience and review of previous studies. Ocul Immunol Inflamm 12:193–201PubMed Perez VL, Papaliodis GN, Chu D, Anzaar F, Christen W, Foster CS (2004) Elevated levels of interleukin 6 in the vitreous fluid of patients with pars planitis and posterior uveitis: the Massachusetts eye & ear experience and review of previous studies. Ocul Immunol Inflamm 12:193–201PubMed
11.
go back to reference El-Asrar AM, Struyf S, Kangave D, Al-Obeidan SS, Opdenakker G, Geboes K, Van Damme J (2011) Cytokine profiles in aqueous humor of patients with different clinical entities of endogenous uveitis. Clin Immunol 139:177–184PubMed El-Asrar AM, Struyf S, Kangave D, Al-Obeidan SS, Opdenakker G, Geboes K, Van Damme J (2011) Cytokine profiles in aqueous humor of patients with different clinical entities of endogenous uveitis. Clin Immunol 139:177–184PubMed
12.
go back to reference Yoshimura T, Sonoda KH, Ohguro N, Ohsugi Y, Ishibashi T, Cua DJ, Kobayashi T, Yoshida H, Yoshimura A (2009) Involvement of Th17 cells and the effect of anti-IL-6 therapy in autoimmune uveitis. Rheumatology 48:347–354PubMed Yoshimura T, Sonoda KH, Ohguro N, Ohsugi Y, Ishibashi T, Cua DJ, Kobayashi T, Yoshida H, Yoshimura A (2009) Involvement of Th17 cells and the effect of anti-IL-6 therapy in autoimmune uveitis. Rheumatology 48:347–354PubMed
13.
go back to reference Kuiper JJ, Mutis T, de Jager W, de Groot-Mijnes JD, Rothova A (2011) Intraocular interleukin-17 and proinflammatory cytokines in HLA-A29-associated birdshot chorioretinopathy. Am J Ophthalmol 152:177–182.e1PubMed Kuiper JJ, Mutis T, de Jager W, de Groot-Mijnes JD, Rothova A (2011) Intraocular interleukin-17 and proinflammatory cytokines in HLA-A29-associated birdshot chorioretinopathy. Am J Ophthalmol 152:177–182.e1PubMed
14.
go back to reference Chen W, Zhao B, Jiang R, Zhang R, Wang Y, Wu H, Gordon L, Chen L (2015) Cytokine expression profile in aqueous humor and sera of patients with acute anterior uveitis. Curr Mol Med 15:543–549PubMed Chen W, Zhao B, Jiang R, Zhang R, Wang Y, Wu H, Gordon L, Chen L (2015) Cytokine expression profile in aqueous humor and sera of patients with acute anterior uveitis. Curr Mol Med 15:543–549PubMed
15.
go back to reference Zhang L, Wan F, Song J, Tang K, Zheng F, Guo J, Guo D, Bi H (2016) Imbalance between Th17 cells and regulatory T cells during monophasic experimental autoimmune uveitis. Inflammation 39:113–122PubMed Zhang L, Wan F, Song J, Tang K, Zheng F, Guo J, Guo D, Bi H (2016) Imbalance between Th17 cells and regulatory T cells during monophasic experimental autoimmune uveitis. Inflammation 39:113–122PubMed
16.
go back to reference Lopalco G, Fabiani C, Sota J, Lucherini OM, Tosi GM, Frediani B, Iannone F, Galeazzi M, Franceschini R, Rigante D, Cantarini L (2017) IL-6 blockade in the management of non-infectious uveitis. Clin Rheumatol 36:1459–1469PubMed Lopalco G, Fabiani C, Sota J, Lucherini OM, Tosi GM, Frediani B, Iannone F, Galeazzi M, Franceschini R, Rigante D, Cantarini L (2017) IL-6 blockade in the management of non-infectious uveitis. Clin Rheumatol 36:1459–1469PubMed
17.
go back to reference Hohki S, Ohguro N, Haruta H, Nakai K, Terabe F, Serada S, Fujimoto M, Nomura S, Kawahata H, Kishimoto T, Naka T (2010) Blockade of interleukin-6 signaling suppresses experimental autoimmune uveoretinitis by the inhibition of inflammatory Th17 responses. Exp Eye Res 91:162–170PubMed Hohki S, Ohguro N, Haruta H, Nakai K, Terabe F, Serada S, Fujimoto M, Nomura S, Kawahata H, Kishimoto T, Naka T (2010) Blockade of interleukin-6 signaling suppresses experimental autoimmune uveoretinitis by the inhibition of inflammatory Th17 responses. Exp Eye Res 91:162–170PubMed
18.
go back to reference Quesada-Masachs E, Caballero CM (2017) Subcutaneous tocilizumab may be less effective than intravenous tocilizumab in the treatment of juvenile idiopathic arthritis-associated uveitis. J Rheumatol 44:260–261PubMed Quesada-Masachs E, Caballero CM (2017) Subcutaneous tocilizumab may be less effective than intravenous tocilizumab in the treatment of juvenile idiopathic arthritis-associated uveitis. J Rheumatol 44:260–261PubMed
19.
go back to reference Calvo-Río V, Santos-Gómez M, Calvo I, González-Fernández MI, López-Montesinos B, Mesquida M, Adán A, Hernández MV, Maíz O, Atanes A, Bravo B, Modesto C, Díaz-Cordovés G, Palmou-Fontana N, Loricera J, González-Vela MC, Demetrio-Pablo R, Hernández JL, González-Gay MA, Blanco R (2017) Anti-Interleukin-6 receptor tocilizumab for severe juvenile idiopathic arthritis-associated uveitis refractory to anti-tumor necrosis factor therapy: a multicenter study of twenty-five patients. Arthritis Rheumatol 69:668–675PubMed Calvo-Río V, Santos-Gómez M, Calvo I, González-Fernández MI, López-Montesinos B, Mesquida M, Adán A, Hernández MV, Maíz O, Atanes A, Bravo B, Modesto C, Díaz-Cordovés G, Palmou-Fontana N, Loricera J, González-Vela MC, Demetrio-Pablo R, Hernández JL, González-Gay MA, Blanco R (2017) Anti-Interleukin-6 receptor tocilizumab for severe juvenile idiopathic arthritis-associated uveitis refractory to anti-tumor necrosis factor therapy: a multicenter study of twenty-five patients. Arthritis Rheumatol 69:668–675PubMed
20.
go back to reference Curragh DS, O'Neill M, McAvoy CE, Rooney M, McLoone E (2018) Pediatric uveitis in a well-defined population: improved outcomes with immunosuppressive therapy. Ocul Immunol Inflamm 26:978–985PubMed Curragh DS, O'Neill M, McAvoy CE, Rooney M, McLoone E (2018) Pediatric uveitis in a well-defined population: improved outcomes with immunosuppressive therapy. Ocul Immunol Inflamm 26:978–985PubMed
21.
go back to reference Tappeiner C, Heinz C, Ganser G, Heiligenhaus A (2012) Is tocilizumab an effective option for treatment of refractory uveitis associated with juvenile idiopathic arthritis? J Rheumatol 39:1294–1295PubMed Tappeiner C, Heinz C, Ganser G, Heiligenhaus A (2012) Is tocilizumab an effective option for treatment of refractory uveitis associated with juvenile idiopathic arthritis? J Rheumatol 39:1294–1295PubMed
22.
go back to reference Tappeiner C, Mesquida M, Adán A, Anton J, Ramanan AV, Carreno E, Mackensen F, Kotaniemi K, de Boer JH, Bou R, de Vicuña CG, Heiligenhaus A (2016) Evidence for tocilizumab as a treatment option in refractory uveitis associated with juvenile idiopathic arthritis. J Rheumatol 43:2183–2188PubMed Tappeiner C, Mesquida M, Adán A, Anton J, Ramanan AV, Carreno E, Mackensen F, Kotaniemi K, de Boer JH, Bou R, de Vicuña CG, Heiligenhaus A (2016) Evidence for tocilizumab as a treatment option in refractory uveitis associated with juvenile idiopathic arthritis. J Rheumatol 43:2183–2188PubMed
23.
go back to reference Mesquida M, Molins B, Llorenç V, Sainz de la Maza M, Adán A (2014) Long-term effects of tocilizumab therapy for refractory uveitis-related macular edema. Ophthalmology 121:2380–2386PubMed Mesquida M, Molins B, Llorenç V, Sainz de la Maza M, Adán A (2014) Long-term effects of tocilizumab therapy for refractory uveitis-related macular edema. Ophthalmology 121:2380–2386PubMed
24.
go back to reference Mesquida M, Molins B, Llorenç V, Hernández MV, Espinosa G, Sainz de la Maza M, Adán A (2018) Twenty-four month follow-up of tocilizumab therapy for refractory uveitis-related macular edema. Retina 38:1361–1370PubMed Mesquida M, Molins B, Llorenç V, Hernández MV, Espinosa G, Sainz de la Maza M, Adán A (2018) Twenty-four month follow-up of tocilizumab therapy for refractory uveitis-related macular edema. Retina 38:1361–1370PubMed
25.
go back to reference Adán A, Mesquida M, Llorenç V, Espinosa G, Molins B, Hernández MV, Pelegrín L (2013) Tocilizumab treatment for refractory uveitis-related cystoid macular edema. Graefes Arch Clin Exp Ophthalmol 251:2627–2632PubMed Adán A, Mesquida M, Llorenç V, Espinosa G, Molins B, Hernández MV, Pelegrín L (2013) Tocilizumab treatment for refractory uveitis-related cystoid macular edema. Graefes Arch Clin Exp Ophthalmol 251:2627–2632PubMed
26.
go back to reference Deuter CME, Zierhut M, Igney-Oertel A, Xenitidis T, Feidt A, Sobolewska B, Stuebiger N, Doycheva D (2017) Tocilizumab in Uveitic macular edema refractory to previous immunomodulatory treatment. Ocul Immunol Inflamm 25:215–220PubMed Deuter CME, Zierhut M, Igney-Oertel A, Xenitidis T, Feidt A, Sobolewska B, Stuebiger N, Doycheva D (2017) Tocilizumab in Uveitic macular edema refractory to previous immunomodulatory treatment. Ocul Immunol Inflamm 25:215–220PubMed
27.
go back to reference Adán A, Mesquida M, Llorenç V, Modesto C (2014) Tocilizumab for retinal vasoproliferative tumor secondary to juvenile idiopathic arthritis-associated uveitis: a case report. Graefes Arch Clin Exp Ophthalmol 252:163–164PubMed Adán A, Mesquida M, Llorenç V, Modesto C (2014) Tocilizumab for retinal vasoproliferative tumor secondary to juvenile idiopathic arthritis-associated uveitis: a case report. Graefes Arch Clin Exp Ophthalmol 252:163–164PubMed
28.
go back to reference Silpa-Archa S, Oray M, Preble JM, Foster CS (2016) Outcome of tocilizumab treatment in refractory ocular inflammatory diseases. Acta Ophthalmol 94:e400–e406PubMed Silpa-Archa S, Oray M, Preble JM, Foster CS (2016) Outcome of tocilizumab treatment in refractory ocular inflammatory diseases. Acta Ophthalmol 94:e400–e406PubMed
29.
go back to reference Tsang AC, Roth J, Gottlieb C (2014) Tocilizumab for severe chronic anterior uveitis associated with juvenile idiopathic arthritis in a pediatric patient. Ocul Immunol Inflamm 22:155–157PubMed Tsang AC, Roth J, Gottlieb C (2014) Tocilizumab for severe chronic anterior uveitis associated with juvenile idiopathic arthritis in a pediatric patient. Ocul Immunol Inflamm 22:155–157PubMed
30.
go back to reference Breitbach M, Tappeiner C, Böhm MR, Zurek-Imhoff B, Heinz C, Thanos S, Ganser G, Heiligenhaus A (2017) Discontinuation of long-term adalimumab treatment in patients with juvenile idiopathic arthritis-associated uveitis. Graefes Arch Clin Exp Ophthalmol 255:171–177PubMed Breitbach M, Tappeiner C, Böhm MR, Zurek-Imhoff B, Heinz C, Thanos S, Ganser G, Heiligenhaus A (2017) Discontinuation of long-term adalimumab treatment in patients with juvenile idiopathic arthritis-associated uveitis. Graefes Arch Clin Exp Ophthalmol 255:171–177PubMed
32.
go back to reference Salek SS, Pradeep A, Guly C, Ramanan AV, Rosenbaum JT (2018) Uveitis and juvenile psoriatic arthritis or psoriasis. Am J Ophthalmol 185:68–74PubMed Salek SS, Pradeep A, Guly C, Ramanan AV, Rosenbaum JT (2018) Uveitis and juvenile psoriatic arthritis or psoriasis. Am J Ophthalmol 185:68–74PubMed
33.
go back to reference Ruperto N, Lovell DJ, Quartier P, Paz E, Rubio-Pérez N, Silva CA, Abud-Mendoza C, Burgos-Vargas R, Gerloni V, Melo-Gomes JA, Saad-Magalhães C, Sztajnbok F, Goldenstein-Schainberg C, Scheinberg M, Calvo Penades I, Fischbach M, Orozco J, Hashkes PJ, Hom C, Jung L, Lepore L, Oliveira S, Wallace CA, Sigal LH, Block AJ, Covucci A, Martini A, Giannini EH, for the Paediatric Rheumatology International Trials Organization (PRINTO) and the Pediatric Rheumatology Collaborative Study Group (PRCSG) (2008) Abatacept in children with juvenile idiopathic arthritis: a randomised, double-blind, placebo-controlled withdrawal trial. Lancet 372:383–391PubMed Ruperto N, Lovell DJ, Quartier P, Paz E, Rubio-Pérez N, Silva CA, Abud-Mendoza C, Burgos-Vargas R, Gerloni V, Melo-Gomes JA, Saad-Magalhães C, Sztajnbok F, Goldenstein-Schainberg C, Scheinberg M, Calvo Penades I, Fischbach M, Orozco J, Hashkes PJ, Hom C, Jung L, Lepore L, Oliveira S, Wallace CA, Sigal LH, Block AJ, Covucci A, Martini A, Giannini EH, for the Paediatric Rheumatology International Trials Organization (PRINTO) and the Pediatric Rheumatology Collaborative Study Group (PRCSG) (2008) Abatacept in children with juvenile idiopathic arthritis: a randomised, double-blind, placebo-controlled withdrawal trial. Lancet 372:383–391PubMed
34.
go back to reference Willermain F, Rosenbaum JT, Bodaghi B, Rosenzweig HL, Childers S, Behrend T, Wildner G, Dick AD (2012) Interplay between innate and adaptive immunity in the development of non-infectious uveitis. Prog Retin Eye Res 31:182–194PubMed Willermain F, Rosenbaum JT, Bodaghi B, Rosenzweig HL, Childers S, Behrend T, Wildner G, Dick AD (2012) Interplay between innate and adaptive immunity in the development of non-infectious uveitis. Prog Retin Eye Res 31:182–194PubMed
35.
36.
go back to reference Lin YT, Wang CT, Gershwin ME, Chiang BL (2011) The pathogenesis of oligoarticular/ polyarticular vs systemic juvenile idiopathic arthritis. Autoimmun Rev 10:482–489PubMed Lin YT, Wang CT, Gershwin ME, Chiang BL (2011) The pathogenesis of oligoarticular/ polyarticular vs systemic juvenile idiopathic arthritis. Autoimmun Rev 10:482–489PubMed
37.
go back to reference Shao H, Woon MD, Nakamura S, Sohn JH, Morton PA, Bora NS, Kaplan HJ (2001) Requirement of B7-mediated costimulation in the induction of experimental autoimmune anterior uveitis. Invest Ophthalmol Vis Sci 42:2016–2021PubMed Shao H, Woon MD, Nakamura S, Sohn JH, Morton PA, Bora NS, Kaplan HJ (2001) Requirement of B7-mediated costimulation in the induction of experimental autoimmune anterior uveitis. Invest Ophthalmol Vis Sci 42:2016–2021PubMed
38.
go back to reference Silver PB, Hathcock KS, Chan CC, Wiggert B, Caspi RR (2000) Blockade of costimulation through B7/CD28 inhibits experimental autoimmune uveoretinitis, but does not induce long-term tolerance. J Immunol 165:5041–5047PubMed Silver PB, Hathcock KS, Chan CC, Wiggert B, Caspi RR (2000) Blockade of costimulation through B7/CD28 inhibits experimental autoimmune uveoretinitis, but does not induce long-term tolerance. J Immunol 165:5041–5047PubMed
39.
go back to reference Ruperto N, Lovell DJ, Quartier P, Paz E, Rubio-Pérez N, Silva CA, Abud-Mendoza C, Burgos-Vargas R, Gerloni V, Melo-Gomes JA, Saad-Magalhães C, Chavez-Corrales J, Huemer C, Kivitz A, Blanco FJ, Foeldvari I, Hofer M, Horneff G, Huppertz HI, Job-Deslandre C, Loy A, Minden K, Punaro M, Nunez AF, Sigal LH, Block AJ, Nys M, Martini A, Giannini EH, Paediatric Rheumatology International Trials Organization and the Pediatric Rheumatology Collaborative Study Group (2010) Long-term safety and efficacy of abatacept in children with juvenile idiopathic arthritis. Arthritis Rheum 62:1792–1802PubMed Ruperto N, Lovell DJ, Quartier P, Paz E, Rubio-Pérez N, Silva CA, Abud-Mendoza C, Burgos-Vargas R, Gerloni V, Melo-Gomes JA, Saad-Magalhães C, Chavez-Corrales J, Huemer C, Kivitz A, Blanco FJ, Foeldvari I, Hofer M, Horneff G, Huppertz HI, Job-Deslandre C, Loy A, Minden K, Punaro M, Nunez AF, Sigal LH, Block AJ, Nys M, Martini A, Giannini EH, Paediatric Rheumatology International Trials Organization and the Pediatric Rheumatology Collaborative Study Group (2010) Long-term safety and efficacy of abatacept in children with juvenile idiopathic arthritis. Arthritis Rheum 62:1792–1802PubMed
40.
go back to reference Birolo C, Zannin ME, Arsenyeva S, Cimaz R, Miserocchi E, Dubko M, Deslandre CJ, Falcini F, Alessio M, La Torre F, Denisova E, Martini G, Nikishina I, Zulian F (2016) Comparable efficacy of Abatacept used as first-line or second-line biological agent for severe juvenile idiopathic arthritis-related uveitis. J Rheumatol 43:2068–2073PubMed Birolo C, Zannin ME, Arsenyeva S, Cimaz R, Miserocchi E, Dubko M, Deslandre CJ, Falcini F, Alessio M, La Torre F, Denisova E, Martini G, Nikishina I, Zulian F (2016) Comparable efficacy of Abatacept used as first-line or second-line biological agent for severe juvenile idiopathic arthritis-related uveitis. J Rheumatol 43:2068–2073PubMed
41.
go back to reference Zulian F, Balzarin M, Falcini F, Martini G, Alessio M, Cimaz R, Cimino L, Zannin ME (2010) Abatacept for severe anti-tumor necrosis factor α refractory juvenile idiopathic arthritis-related uveitis. Arthritis Care Res (Hoboken) 62:821–825 Zulian F, Balzarin M, Falcini F, Martini G, Alessio M, Cimaz R, Cimino L, Zannin ME (2010) Abatacept for severe anti-tumor necrosis factor α refractory juvenile idiopathic arthritis-related uveitis. Arthritis Care Res (Hoboken) 62:821–825
42.
go back to reference Angeles-Han S, Flynn T, Lehman T (2008) Abatacept for refractory juvenile idiopathic arthritis-associated uveitis- a case report. J Rheumatol 35:1897–1898PubMed Angeles-Han S, Flynn T, Lehman T (2008) Abatacept for refractory juvenile idiopathic arthritis-associated uveitis- a case report. J Rheumatol 35:1897–1898PubMed
43.
go back to reference Alpigiani MG, Salvati P, Vannati M, Callegari S, Trovato F, Rossi R, Gamba S, Lorini R (2010) Abatacept for severe anti TNF-alpha refractory JIA-associated uveitis: a case report. 17th Pediatric Rheumatology European Society Congress. September 9-12 València, Spain Alpigiani MG, Salvati P, Vannati M, Callegari S, Trovato F, Rossi R, Gamba S, Lorini R (2010) Abatacept for severe anti TNF-alpha refractory JIA-associated uveitis: a case report. 17th Pediatric Rheumatology European Society Congress. September 9-12 València, Spain
44.
go back to reference Elhai M, Deslandre CJ, Kahan A (2011) Abatacept for refractory juvenile idiopathic arthritis-associated uveitis: two new cases. Comment on the article by Zulian et al. Arthritis Care Res (Hoboken) 63:307–308 author reply 308 Elhai M, Deslandre CJ, Kahan A (2011) Abatacept for refractory juvenile idiopathic arthritis-associated uveitis: two new cases. Comment on the article by Zulian et al. Arthritis Care Res (Hoboken) 63:307–308 author reply 308
45.
go back to reference Kenawy N, Cleary G, Mewar D, Beare N, Chandna A, Pearce I (2011) Abatacept: a potential therapy in refractory cases of juvenile idiopathic arthritis-associated uveitis. Graefes Arch Clin Exp Ophthalmol 249:297–300PubMed Kenawy N, Cleary G, Mewar D, Beare N, Chandna A, Pearce I (2011) Abatacept: a potential therapy in refractory cases of juvenile idiopathic arthritis-associated uveitis. Graefes Arch Clin Exp Ophthalmol 249:297–300PubMed
46.
go back to reference Tappeiner C, Miserocchi E, Bodaghi B, Kotaniemi K, Mackensen F, Gerloni V, Quartier P, Lutz T, Heiligenhaus A (2015) Abatacept in the treatment of severe, longstanding, and refractory uveitis associated with juvenile idiopathic arthritis. J Rheumatol 42:706–711PubMed Tappeiner C, Miserocchi E, Bodaghi B, Kotaniemi K, Mackensen F, Gerloni V, Quartier P, Lutz T, Heiligenhaus A (2015) Abatacept in the treatment of severe, longstanding, and refractory uveitis associated with juvenile idiopathic arthritis. J Rheumatol 42:706–711PubMed
47.
go back to reference MacIsaac J, Siddiqui R, Jamula E, Li N, Baker S, Webert KE, Evanovitch D, Heddle NM, Arnold DM (2018) Systematic review of rituximab for autoimmune diseases: a potential alternative to intravenous immune globulin. Transfusion 58:2729–2735PubMed MacIsaac J, Siddiqui R, Jamula E, Li N, Baker S, Webert KE, Evanovitch D, Heddle NM, Arnold DM (2018) Systematic review of rituximab for autoimmune diseases: a potential alternative to intravenous immune globulin. Transfusion 58:2729–2735PubMed
48.
go back to reference Barnes MG, Grom AA, Thompson SD, Griffin TA, Pavlidis P, Itert L, Fall N, Sowders DP, Hinze CH, Aronow BJ, Luyrink LK, Srivastava S, Ilowite NT, Gottlieb BS, Olson JC, Sherry DD, Glass DN, Colbert RA (2009) Subtype-specific peripheral blood gene expression profiles in recent-onset juvenile idiopathic arthritis. Arthritis Rheum 60:2102–2112PubMedPubMedCentral Barnes MG, Grom AA, Thompson SD, Griffin TA, Pavlidis P, Itert L, Fall N, Sowders DP, Hinze CH, Aronow BJ, Luyrink LK, Srivastava S, Ilowite NT, Gottlieb BS, Olson JC, Sherry DD, Glass DN, Colbert RA (2009) Subtype-specific peripheral blood gene expression profiles in recent-onset juvenile idiopathic arthritis. Arthritis Rheum 60:2102–2112PubMedPubMedCentral
49.
go back to reference Kazkaz H, Isenberg D (2004) Anti B cell therapy (rituximab) in the treatment of autoimmune diseases. Curr Opin Pharmacol 4:398–402PubMed Kazkaz H, Isenberg D (2004) Anti B cell therapy (rituximab) in the treatment of autoimmune diseases. Curr Opin Pharmacol 4:398–402PubMed
50.
go back to reference Miserocchi E, Modorati G (2012) Rituximab for noninfectious uveitis. Dev Ophthalmol 51:98–109PubMed Miserocchi E, Modorati G (2012) Rituximab for noninfectious uveitis. Dev Ophthalmol 51:98–109PubMed
51.
go back to reference Sfikakis PP, Souliotis VL, Fragiadaki KG, Moutsopoulos HM, Boletis JN, Theofilopoulos AN (2007) Increased expression of the FoxP3 functional marker of regulatory T cells following B cell depletion with rituximab in patients with lupus nephritis. Clin Immunol 123:66–73PubMed Sfikakis PP, Souliotis VL, Fragiadaki KG, Moutsopoulos HM, Boletis JN, Theofilopoulos AN (2007) Increased expression of the FoxP3 functional marker of regulatory T cells following B cell depletion with rituximab in patients with lupus nephritis. Clin Immunol 123:66–73PubMed
52.
go back to reference Catzola V, Battaglia A, Buzzonetti A, Fossati M, Scuderi F, Fattorossi A, Evoli A (2013) Changes in regulatory T cells after rituximab in two patients with refractory myasthenia gravis. J Neurol 260:2163–2165PubMed Catzola V, Battaglia A, Buzzonetti A, Fossati M, Scuderi F, Fattorossi A, Evoli A (2013) Changes in regulatory T cells after rituximab in two patients with refractory myasthenia gravis. J Neurol 260:2163–2165PubMed
53.
go back to reference Hultin LE, Hausner MA, Hultin PM, Giorgi JV (1993) CD20 (pan-B cell) antigen is expressed at a low level on a subpopulation of human T lymphocytes. Cytometry 14:196–204PubMed Hultin LE, Hausner MA, Hultin PM, Giorgi JV (1993) CD20 (pan-B cell) antigen is expressed at a low level on a subpopulation of human T lymphocytes. Cytometry 14:196–204PubMed
54.
go back to reference 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 (Oxford) 50:1390–1394 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 (Oxford) 50:1390–1394
55.
go back to reference Miserocchi E, Pontikaki I, Modorati G, Bandello F, Meroni PL, Gerloni V (2011) Rituximab for uveitis. Ophthalmology 118:223–224PubMed Miserocchi E, Pontikaki I, Modorati G, Bandello F, Meroni PL, Gerloni V (2011) Rituximab for uveitis. Ophthalmology 118:223–224PubMed
56.
go back to reference Miserocchi E, Modorati G, Berchicci L, Pontikaki I, Meroni P, Gerloni V (2016) Long-term treatment with rituximab in severe juvenile idiopathic arthritis-associated uveitis. Br J Ophthalmol 100:782–786PubMed Miserocchi E, Modorati G, Berchicci L, Pontikaki I, Meroni P, Gerloni V (2016) Long-term treatment with rituximab in severe juvenile idiopathic arthritis-associated uveitis. Br J Ophthalmol 100:782–786PubMed
57.
go back to reference Pelegrin L, Jakob E, Schmidt-Bacher A, Schwenger V, Becker M, Max R, Lorenz HM, Mackensen F (2014) Experiences with rituximab for the treatment of autoimmune diseases with ocular involvement. J Rheumatol 41:84–90PubMed Pelegrin L, Jakob E, Schmidt-Bacher A, Schwenger V, Becker M, Max R, Lorenz HM, Mackensen F (2014) Experiences with rituximab for the treatment of autoimmune diseases with ocular involvement. J Rheumatol 41:84–90PubMed
58.
go back to reference Cohen SB, Emery P, Greenwald MW, Dougados M, Furie RA, Genovese MC, Keystone EC, Loveless JE, Burmester GR, Cravets MW, Hessey EW, Shaw T, Totoritis MC, REFLEX Trial Group (2006) Rituximab for rheumatoid arthritis refractory to anti-tumor necrosis factor therapy: results of a multicenter, randomized, double-blind, placebo-controlled, phase III trial evaluating primary efficacy and safety at twenty-four weeks. Arthritis Rheum 54:2793–2806PubMed Cohen SB, Emery P, Greenwald MW, Dougados M, Furie RA, Genovese MC, Keystone EC, Loveless JE, Burmester GR, Cravets MW, Hessey EW, Shaw T, Totoritis MC, REFLEX Trial Group (2006) Rituximab for rheumatoid arthritis refractory to anti-tumor necrosis factor therapy: results of a multicenter, randomized, double-blind, placebo-controlled, phase III trial evaluating primary efficacy and safety at twenty-four weeks. Arthritis Rheum 54:2793–2806PubMed
59.
go back to reference Kimby E (2005) Tolerability and safety of rituximab (MabThera). Cancer Treat Rev 31:456–473PubMed Kimby E (2005) Tolerability and safety of rituximab (MabThera). Cancer Treat Rev 31:456–473PubMed
60.
go back to reference Guex-Crosier Y, Raber J, Chan CC, Kriete MS, Benichou J, Pilson RS, Kerwin JA, Waldmann TA, Hakimi J, Roberge FG (1997) Humanized antibodies against the α-chain of the IL-2 receptor and against the beta-chain shared by the IL-2 and IL-15 receptors in a monkey uveitis model of autoimmune diseases. J Immunol 158:452–458PubMed Guex-Crosier Y, Raber J, Chan CC, Kriete MS, Benichou J, Pilson RS, Kerwin JA, Waldmann TA, Hakimi J, Roberge FG (1997) Humanized antibodies against the α-chain of the IL-2 receptor and against the beta-chain shared by the IL-2 and IL-15 receptors in a monkey uveitis model of autoimmune diseases. J Immunol 158:452–458PubMed
61.
go back to reference Gallagher M, Quinones K, Cervantes-Castañeda RA, Yilmaz T, Foster CS (2007) Biological response modifier therapy for refractory childhood uveitis. Br J Ophthalmol 91:1341–1344PubMedPubMedCentral Gallagher M, Quinones K, Cervantes-Castañeda RA, Yilmaz T, Foster CS (2007) Biological response modifier therapy for refractory childhood uveitis. Br J Ophthalmol 91:1341–1344PubMedPubMedCentral
62.
go back to reference Sen HN, Levy-Clarke G, Faia LJ, Li Z, Yeh S, Barron KS, Ryan JG, Hammel K, Nussenblatt RB (2009) High-dose daclizumab for the treatment of juvenile idiopathic arthritis-associated active anterior uveitis. Am J Ophthalmol 148:696–703.e1PubMedPubMedCentral Sen HN, Levy-Clarke G, Faia LJ, Li Z, Yeh S, Barron KS, Ryan JG, Hammel K, Nussenblatt RB (2009) High-dose daclizumab for the treatment of juvenile idiopathic arthritis-associated active anterior uveitis. Am J Ophthalmol 148:696–703.e1PubMedPubMedCentral
63.
go back to reference Nussenblatt RB, Fortin E, Schiffman R, Rizzo L, Smith J, Van Veldhuisen P, Sran P, Yaffe A, Goldman CK, Waldmann TA, Whitcup SM (1999) Treatment of noninfectious intermediate and posterior uveitis with the humanized anti-tac mAb: a phase I/II clinical trial. Proc Natl Acad Sci U S A 96:7462–7466PubMedPubMedCentral Nussenblatt RB, Fortin E, Schiffman R, Rizzo L, Smith J, Van Veldhuisen P, Sran P, Yaffe A, Goldman CK, Waldmann TA, Whitcup SM (1999) Treatment of noninfectious intermediate and posterior uveitis with the humanized anti-tac mAb: a phase I/II clinical trial. Proc Natl Acad Sci U S A 96:7462–7466PubMedPubMedCentral
64.
go back to reference Nussenblatt RB, Peterson JS, Foster CS, Rao NA, See RF, Letko E, Buggage RR (2005) Initial evaluation of subcutaneous daclizumab treatments for noninfectious uveitis: a multicenter noncomparative interventional case series. Ophthalmology 112:764–770PubMed Nussenblatt RB, Peterson JS, Foster CS, Rao NA, See RF, Letko E, Buggage RR (2005) Initial evaluation of subcutaneous daclizumab treatments for noninfectious uveitis: a multicenter noncomparative interventional case series. Ophthalmology 112:764–770PubMed
65.
go back to reference Fabiani C, Sota J, Tosi GM, Franceschini R, Frediani B, Galeazzi M, Rigante D, Cantarini L (2017) The emerging role of interleukin (IL)-1 in the pathogenesis and treatment of inflammatory and degenerative eye diseases. Clin Rheumatol 36:2307–2318PubMed Fabiani C, Sota J, Tosi GM, Franceschini R, Frediani B, Galeazzi M, Rigante D, Cantarini L (2017) The emerging role of interleukin (IL)-1 in the pathogenesis and treatment of inflammatory and degenerative eye diseases. Clin Rheumatol 36:2307–2318PubMed
66.
go back to reference Brambilla A, Caputo R, Cimaz R, Simonini G (2016) Canakinumab for childhood sight-threatening refractory uveitis: a case series. J Rheumatol 43:1445–1447PubMed Brambilla A, Caputo R, Cimaz R, Simonini G (2016) Canakinumab for childhood sight-threatening refractory uveitis: a case series. J Rheumatol 43:1445–1447PubMed
67.
68.
go back to reference Pepple KL, Lin P (2018) Targeting Interleukin-23 in the treatment of noninfectious uveitis. Ophthalmology 125:1977–1983PubMedPubMedCentral Pepple KL, Lin P (2018) Targeting Interleukin-23 in the treatment of noninfectious uveitis. Ophthalmology 125:1977–1983PubMedPubMedCentral
69.
go back to reference Wu SA, Yeh KW, Lee WI, Yao TC, Huang JL (2016) Persistent improper upregulation of Th17 and TReg cells in patients with juvenile idiopathic arthritis. J Microbiol Immunol Infect 49:402–408PubMed Wu SA, Yeh KW, Lee WI, Yao TC, Huang JL (2016) Persistent improper upregulation of Th17 and TReg cells in patients with juvenile idiopathic arthritis. J Microbiol Immunol Infect 49:402–408PubMed
70.
go back to reference Constantin T, Foeldvari I, Anton J, de Boer J, Czitrom-Guillaume S, Edelsten C, Gepstein R, Heiligenhaus A, Pilkington CA, Simonini G, Uziel Y, Vastert SJ, Wulffraat NM, Haasnoot AM, Walscheid K, Pálinkás A, Pattani R, Györgyi Z, Kozma R, Boom V, Ponyi A, Ravelli A, Ramanan AV (2018) Consensus-based recommendations for the management of uveitis associated with juvenile idiopathic arthritis: the SHARE initiative. Ann Rheum Dis 77:1107–1117PubMedPubMedCentral Constantin T, Foeldvari I, Anton J, de Boer J, Czitrom-Guillaume S, Edelsten C, Gepstein R, Heiligenhaus A, Pilkington CA, Simonini G, Uziel Y, Vastert SJ, Wulffraat NM, Haasnoot AM, Walscheid K, Pálinkás A, Pattani R, Györgyi Z, Kozma R, Boom V, Ponyi A, Ravelli A, Ramanan AV (2018) Consensus-based recommendations for the management of uveitis associated with juvenile idiopathic arthritis: the SHARE initiative. Ann Rheum Dis 77:1107–1117PubMedPubMedCentral
71.
go back to reference Ravelli A, Consolaro A, Horneff G, Laxer RM, Lovell DJ, Wulffraat NM, Akikusa JD, Al-Mayouf SM, Antón J, Avcin T, Berard RA, Beresford MW, Burgos-Vargas R, Cimaz R, De Benedetti F, Demirkaya E, Foell D, Itoh Y, Lahdenne P, Morgan EM, Quartier P, Ruperto N, Russo R, Saad-Magalhães C, Sawhney S, Scott C, Shenoi S, Swart JF, Uziel Y, Vastert SJ, Smolen JS (2018) Treating juvenile idiopathic arthritis to target: recommendations of an international task force. Ann Rheum Dis 77:819–828PubMed Ravelli A, Consolaro A, Horneff G, Laxer RM, Lovell DJ, Wulffraat NM, Akikusa JD, Al-Mayouf SM, Antón J, Avcin T, Berard RA, Beresford MW, Burgos-Vargas R, Cimaz R, De Benedetti F, Demirkaya E, Foell D, Itoh Y, Lahdenne P, Morgan EM, Quartier P, Ruperto N, Russo R, Saad-Magalhães C, Sawhney S, Scott C, Shenoi S, Swart JF, Uziel Y, Vastert SJ, Smolen JS (2018) Treating juvenile idiopathic arthritis to target: recommendations of an international task force. Ann Rheum Dis 77:819–828PubMed
72.
go back to reference Thorne JE, Woreta F, Kedhar SR, Dunn JP, Jabs DA (2007) Juvenile idiopathic arthritis-associated uveitis: incidence of ocular complications and visual acuity loss. Am J Ophthalmol 143:840–846PubMed Thorne JE, Woreta F, Kedhar SR, Dunn JP, Jabs DA (2007) Juvenile idiopathic arthritis-associated uveitis: incidence of ocular complications and visual acuity loss. Am J Ophthalmol 143:840–846PubMed
73.
go back to reference Levy-Clarke G, Jabs DA, Read RW, Rosenbaum JT, Vitale A, Van Gelder RN (2014) Expert panel recommendations for the use of anti-tumor necrosis factor biologic agents in patients with ocular inflammatory disorders. Ophthalmology 121:785–796PubMed Levy-Clarke G, Jabs DA, Read RW, Rosenbaum JT, Vitale A, Van Gelder RN (2014) Expert panel recommendations for the use of anti-tumor necrosis factor biologic agents in patients with ocular inflammatory disorders. Ophthalmology 121:785–796PubMed
74.
go back to reference Simonini G, Druce K, Cimaz R, Macfarlane GJ, Jones GT (2014) Current evidence of anti-tumor necrosis factor α treatment efficacy in childhood chronic uveitis: a systematic review and meta-analysis approach of individual drugs. Arthritis Care Res 66:1073–1084 Simonini G, Druce K, Cimaz R, Macfarlane GJ, Jones GT (2014) Current evidence of anti-tumor necrosis factor α treatment efficacy in childhood chronic uveitis: a systematic review and meta-analysis approach of individual drugs. Arthritis Care Res 66:1073–1084
75.
go back to reference Ramanan AV, Dick AD, Jones AP, McKay A, Williamson PR, Compeyrot-Lacassagne S, Hardwick B, Hickey H, Hughes D, Woo P, Benton D, Edelsten C, Beresford MW, SYCAMORE Study Group (2017) Adalimumab plus methotrexate for uveitis in juvenile idiopathic arthritis. N Engl J Med 376:1637–1646PubMed Ramanan AV, Dick AD, Jones AP, McKay A, Williamson PR, Compeyrot-Lacassagne S, Hardwick B, Hickey H, Hughes D, Woo P, Benton D, Edelsten C, Beresford MW, SYCAMORE Study Group (2017) Adalimumab plus methotrexate for uveitis in juvenile idiopathic arthritis. N Engl J Med 376:1637–1646PubMed
76.
go back to reference Leinonen ST, Aalto K, Kotaniemi KM, Kivelä TT (2017) Anti-adalimumab antibodies in juvenile idiopathic arthritis-related uveitis. Clin Exp Rheumatol 35:1043–1046PubMed Leinonen ST, Aalto K, Kotaniemi KM, Kivelä TT (2017) Anti-adalimumab antibodies in juvenile idiopathic arthritis-related uveitis. Clin Exp Rheumatol 35:1043–1046PubMed
77.
go back to reference Skrabl-Baumgartner A, Erwa W, Muntean W, Jahnel J (2015) Anti-adalimumab antibodies in juvenile idiopathic arthritis: frequent association with loss of response. Scand J Rheumatol 44:359–362PubMed Skrabl-Baumgartner A, Erwa W, Muntean W, Jahnel J (2015) Anti-adalimumab antibodies in juvenile idiopathic arthritis: frequent association with loss of response. Scand J Rheumatol 44:359–362PubMed
78.
go back to reference Correll CK, Bullock DR, Cafferty RM, Vehe RK (2018) Safety of weekly adalimumab in the treatment of juvenile idiopathic arthritis and pediatric chronic uveitis. Clin Rheumatol 37:549–553PubMed Correll CK, Bullock DR, Cafferty RM, Vehe RK (2018) Safety of weekly adalimumab in the treatment of juvenile idiopathic arthritis and pediatric chronic uveitis. Clin Rheumatol 37:549–553PubMed
79.
go back to reference Dhingra N, Morgan J, Dick AD (2009) Switching biologic agents for uveitis. Eye 23:1868–1870PubMed Dhingra N, Morgan J, Dick AD (2009) Switching biologic agents for uveitis. Eye 23:1868–1870PubMed
80.
go back to reference Miserocchi E, Modorati G, Pontikaki I, Meroni PL, Gerloni V (2014) Long-term treatment with golimumab for severe uveitis. Ocul Immunol Inflamm 22:90–95PubMed Miserocchi E, Modorati G, Pontikaki I, Meroni PL, Gerloni V (2014) Long-term treatment with golimumab for severe uveitis. Ocul Immunol Inflamm 22:90–95PubMed
Metadata
Title
Treating juvenile idiopathic arthritis (JIA)-related uveitis beyond TNF-α inhibition: a narrative review
Authors
Carla Gaggiano
Donato Rigante
Gian Marco Tosi
Antonio Vitale
Bruno Frediani
Salvatore Grosso
Claudia Fabiani
Luca Cantarini
Publication date
01-02-2020
Publisher
Springer London
Published in
Clinical Rheumatology / Issue 2/2020
Print ISSN: 0770-3198
Electronic ISSN: 1434-9949
DOI
https://doi.org/10.1007/s10067-019-04763-3

Other articles of this Issue 2/2020

Clinical Rheumatology 2/2020 Go to the issue