Remission maintenance in ANCA-associated vasculitis: does one size fit all?

References

• Jennette JC, Falk RJ, Bacon PA, et al. 2012 Revised International chapel hill consensus conference nomenclature of vasculitides. Arthritis Rheumatol. 2013;65:1–11. 2012
   PubMed Web of Science ®Google Scholar
• Chen M, Kallenberg CG. ANCA-associated vasculitides–advances in pathogenesis and treatment. Nat Rev Rheumatol. 2010;6:653–664.
   PubMed Web of Science ®Google Scholar
• Schonermarck U, Csernok E, Gross WL. Pathogenesis of anti-neutrophil cytoplasmic antibody-associated vasculitis: challenges and solutions 2014. NTD. 2015;30:46–52.
   PubMed Web of Science ®Google Scholar
• Robson J, Doll H, Suppiah R, et al. Damage in the anca-associated vasculitides: long-term data from the European vasculitis study group (EUVAS) therapeutic trials. Ann Rheum Dis. 2015;74:177–184.
   PubMed Web of Science ®Google Scholar
• Westman KW, Bygren PG, Olsson H, et al. Relapse rate, renal survival, and cancer morbidity in patients with Wegener’s granulomatosis or microscopic polyangiitis with renal involvement. JASN. 1998;9:842–852.
   Web of Science ®Google Scholar
• McDonough AK, Curtis JR, Saag KG. The epidemiology of glucocorticoid-associated adverse events. Curr Opin Rheumatol. 2008;20:131–137.
   PubMed Web of Science ®Google Scholar
• Robson J, Doll H, Suppiah R, et al. Glucocorticoid treatment and damage in the anti-neutrophil cytoplasm antibody-associated vasculitides: long-term data from the European vasculitis study group trials. Rheumatology (Oxford). 2015;54:471–481.
   PubMed Web of Science ®Google Scholar
• Fauci AS, Haynes BF, Katz P, et al. Wegener’s granulomatosis: prospective clinical and therapeutic experience with 85 patients for 21 years. Ann Intern Med. 1983;98:76–85.
   PubMed Web of Science ®Google Scholar
• Jayne D, Rasmussen N, Andrassy K, et al. A randomized trial of maintenance therapy for vasculitis associated with antineutrophil cytoplasmic autoantibodies. N Engl J Med. 2003;349:36–44.
   PubMed Web of Science ®Google Scholar
• Booth AD, Almond MK, Burns A, et al. Outcome of ANCA-associated renal vasculitis: a 5-year retrospective study. Am J Kidney Dis. 2003;41:776–784.
   PubMed Web of Science ®Google Scholar
• Specks U, Merkel PA, Seo P, et al. Efficacy of remission-induction regimens for ANCA-associated vasculitis. N Engl J Med. 2013;369:417–427.
   PubMed Web of Science ®Google Scholar
• Lionaki S, Blyth ER, Hogan SL, et al. Classification of antineutrophil cytoplasmic autoantibody vasculitides: the role of antineutrophil cytoplasmic autoantibody specificity for myeloperoxidase or proteinase 3 in disease recognition and prognosis. Arthritis Rheumatol. 2012;64:3452–3462.
   PubMed Web of Science ®Google Scholar
• Yates M, Watts RA, Bajema IM, et al. EULAR/ERA-EDTA recommendations for the management of ANCA-associated vasculitis. Ann Rheum Dis. 2016;75:1583–1594.
   PubMed Web of Science ®Google Scholar
• Stone JH, Merkel PA, Spiera R, et al. Rituximab versus cyclophosphamide for ANCA-associated vasculitis. N Engl J Med. 2010;363:221–232.
   PubMed Web of Science ®Google Scholar
• Wegener’s Granulomatosis Etanercept Trial (WGET) Research Group. Etanercept plus standard therapy for Wegener’s granulomatosis. N Engl J Med. 2005;352:351–361.
   PubMed Web of Science ®Google Scholar
• Harper L, Morgan MD, Walsh M, et al. Pulse versus daily oral cyclophosphamide for induction of remission in ANCA-associated vasculitis: long-term follow-up. Ann Rheum Dis. 2012;71:955–960.
   PubMed Web of Science ®Google Scholar
• Hoffman GS, Kerr GS, Leavitt RY, et al. Wegener granulomatosis: an analysis of 158 patients. Ann Intern Med. 1992;116:488–498.
   PubMed Web of Science ®Google Scholar
• Jones RB, Tervaert JW, Hauser T, et al. Rituximab versus cyclophosphamide in ANCA-associated renal vasculitis. N Engl J Med. 2010;363:211–220.
   PubMed Web of Science ®Google Scholar
• Davies DJ, Moran JE, Niall JF, et al. Segmental necrotising glomerulonephritis with antineutrophil antibody: possible arbovirus aetiology? Br Med J (Clinical Research ed). 1982;285:606.
   PubMed Web of Science ®Google Scholar
• Hall JB, Wadham BM, Wood CJ, et al. Vasculitis and glomerulonephritis: a subgroup with an antineutrophil cytoplasmic antibody. Aust NZ J Med. 1984;14:277–278.
   PubMedGoogle Scholar
• van der Woude FJ, Rasmussen N, Lobatto S, et al. Autoantibodies against neutrophils and monocytes: tool for diagnosis and marker of disease activity in Wegener’s granulomatosis. Lancet. 1985;1:425–429.
   PubMed Web of Science ®Google Scholar
• Nolle B, Specks U, Ludemann J, et al. Anticytoplasmic autoantibodies: their immunodiagnostic value in Wegener granulomatosis. Ann Intern Med. 1989;111:28–40.
   PubMed Web of Science ®Google Scholar
• Tervaert JW, van der Woude FJ, Fauci AS, et al. Association between active Wegener’s granulomatosis and anticytoplasmic antibodies. Arch Internal Med. 1989;149:2461–2465.
   PubMed Web of Science ®Google Scholar
• Tervaert JW, Huitema MG, Hene RJ, et al. Prevention of relapses in Wegener’s granulomatosis by treatment based on antineutrophil cytoplasmic antibody titre. Lancet. 1990;336(8717):709–711.
   PubMed Web of Science ®Google Scholar
• Talar-Williams C, Hijazi YM, Walther MM, et al. Cyclophosphamide-induced cystitis and bladder cancer in patients with Wegener granulomatosis. Ann Intern Med. 1996;124:477–484.
   PubMed Web of Science ®Google Scholar
• Stegeman CA, Tervaert JW, de Jong PE, et al. Trimethoprim-sulfamethoxazole (co-trimoxazole) for the prevention of relapses of Wegener’s granulomatosis. Dutch Co-Trimoxazole Wegener study group. New Engl J Med. 1996;335:16–20.
   PubMed Web of Science ®Google Scholar
• Hogan SL, Falk RJ, Chin H, et al. Predictors of relapse and treatment resistance in antineutrophil cytoplasmic antibody-associated small-vessel vasculitis. Ann Intern Med. 2005;143:621–631.
   PubMed Web of Science ®Google Scholar
• de Groot K, Harper L, Jayne DR, et al. Pulse versus daily oral cyclophosphamide for induction of remission in antineutrophil cytoplasmic antibody-associated vasculitis: a randomized trial. Ann Intern Med. 2009;150:670–680.
   PubMed Web of Science ®Google Scholar
• Langford CA, Talar-Williams C, Barron KS, et al. A staged approach to the treatment of Wegener’s granulomatosis: induction of remission with glucocorticoids and daily cyclophosphamide switching to methotrexate for remission maintenance. Arthritis Rheumatol. 1999;42:2666–2673.
   PubMed Web of Science ®Google Scholar
• Maritati F, Alberici F, Oliva E, et al. Methotrexate versus cyclophosphamide for remission maintenance in ANCA-associated vasculitis: A randomised trial. PLoS One. 2017;12:0185880.
   Web of Science ®Google Scholar
• De Groot K, Rasmussen N, Bacon PA, et al. Randomized trial of cyclophosphamide versus methotrexate for induction of remission in early systemic antineutrophil cytoplasmic antibody-associated vasculitis. Arthritis Rheumatol. 2005;52:2461–2469.
   PubMed Web of Science ®Google Scholar
• Pagnoux C, Mahr A, Hamidou MA, et al. Azathioprine or methotrexate maintenance for ANCA-associated vasculitis. N Engl J Med. 2008;359:2790–2803.
   PubMed Web of Science ®Google Scholar
• Karras A, Pagnoux C, Haubitz M, et al. Randomised controlled trial of prolonged treatment in the remission phase of ANCA-associated vasculitis. Ann Rheumatic Dis. 2017;76:1662–1668.
   PubMed Web of Science ®Google Scholar
• Sanders JS, de Joode AA, DeSevaux RG, et al. Extended versus standard azathioprine maintenance therapy in newly diagnosed proteinase-3 anti-neutrophil cytoplasmic antibody-associated vasculitis patients who remain cytoplasmic anti-neutrophil cytoplasmic antibody-positive after induction of remission: a randomized clinical trial. NTD. 2016;31:1453–1459.
   PubMed Web of Science ®Google Scholar
• de Joode AAE, Puéchal X, Guillevin LP, et al. Long term azathioprine maintenance therapy in ANCA-associated vasculitis: combined results of long-term follow-up data. Rheumatology. 2017;56:1894–1901.
   PubMed Web of Science ®Google Scholar
• Silva F, Specks U, Kalra S, et al. Mycophenolate Mofetil for induction and maintenance of remission in microscopic polyangiitis with mild to moderate renal involvement—A prospective, open-label pilot trial. CJASN. 2010;5:445–453.
   PubMed Web of Science ®Google Scholar
• Hu W, Liu C, Xie H, et al. Mycophenolate mofetil versus cyclophosphamide for inducing remission of ANCA vasculitis with moderate renal involvement. NTD. 2008;23:1307–1312.
   PubMed Web of Science ®Google Scholar
• Hiemstra TF, Walsh M, Mahr A, et al. Mycophenolate mofetil vs azathioprine for remission maintenance in antineutrophil cytoplasmic antibody-associated vasculitis: a randomized controlled trial. Jama. 2010;304:2381–2388.
   PubMed Web of Science ®Google Scholar
• Jones RB, Hiemstra TF, Ballarin J, et al. Mycophenolate mofetil versus cyclophosphamide for remission induction in ANCA-associated vasculitis: a randomised, non-inferiority trial. Ann Rheumatic Dis. 2019;78:399–405.
   PubMed Web of Science ®Google Scholar
• Lee T, Gasim A, Derebail VK, et al. Predictors of treatment outcomes in ANCA-associated vasculitis with severe kidney failure. CJASN. 2014;9:905–913.
   PubMed Web of Science ®Google Scholar
• de Joode AA, Sanders JS, Stegeman CA. Renal survival in proteinase 3 and myeloperoxidase ANCA-associated systemic vasculitis. CJASN. 2013;8:1709–1717.
   PubMed Web of Science ®Google Scholar
• Specks U. Accurate relapse prediction in ANCA-associated vasculitis-the search for the Holy Grail. JASN. 2015;26(3):505–507.
   Web of Science ®Google Scholar
• Cornec D, Cornec-Le Gall E, Fervenza FC, et al. ANCA-associated vasculitis - clinical utility of using ANCA specificity to classify patients. Nat Rev Rheumatol. 2016;12:570–579.
   PubMed Web of Science ®Google Scholar
• Geetha D, Specks U, Stone JH, et al. Rituximab versus cyclophosphamide for ANCA-associated vasculitis with renal involvement. JASN. 2015;26:976–985.
   Web of Science ®Google Scholar
• Unizony S, Villarreal M, Miloslavsky EM, et al. Clinical outcomes of treatment of anti-neutrophil cytoplasmic antibody (ANCA)-associated vasculitis based on ANCA type. Ann Rheum Dis. 2016;75:1166–1169.
   PubMed Web of Science ®Google Scholar
• Nachman PH, Hogan SL, Jennette JC, et al. Treatment response and relapse in antineutrophil cytoplasmic autoantibody-associated microscopic polyangiitis and glomerulonephritis. JASN. 1996;7:33–39.
   Web of Science ®Google Scholar
• Franssen CF, Gans RO, Arends B, et al. Differences between anti-myeloperoxidase- and anti-proteinase 3-associated renal disease. Kidney Int. 1995;47:193–199.
   PubMed Web of Science ®Google Scholar
• Walsh M, Flossmann O, Berden A, et al. Risk factors for relapse of antineutrophil cytoplasmic antibody-associated vasculitis. Arthritis Rheumatol. 2012;64:542–548.
   PubMed Web of Science ®Google Scholar
• Lyons PA, Rayner TF, Trivedi S, et al. Genetically distinct subsets within ANCA-associated vasculitis. N Engl J Med. 2012;367:214–223.
   PubMed Web of Science ®Google Scholar
• Mukhtyar C, Flossmann O, Hellmich B, et al. Outcomes from studies of antineutrophil cytoplasm antibody associated vasculitis: a systematic review by the European league against rheumatism systemic vasculitis task force. Ann Rheum Dis. 2008;67:1004–1010.
   PubMed Web of Science ®Google Scholar
• Merkel PA, Xie G, Monach PA, et al. Identification of functional and expression polymorphisms associated with risk for anti-neutrophil cytoplasmic autoantibody-associated vasculitis. Arthritis Rheumatol. 2017;69:1054–1066.
   PubMed Web of Science ®Google Scholar
• Alberici F, Smith RM, Fonseca M, et al. Association of a TNFSF13B (BAFF) regulatory region single nucleotide polymorphism with response to rituximab in antineutrophil cytoplasmic antibody-associated vasculitis. J Allergy Clin Immunol. 2017;139:1684.e10–1687.e10.
   PubMed Web of Science ®Google Scholar
• Berti A, Warner R, Johnson K, et al. Circulating cytokine profiles and antineutrophil cytoplasmic antibody specificity in patients with antineutrophil cytoplasmic antibody-associated vasculitis. Arthritis Rheumatol. 2018;70:1114–1121.
   PubMed Web of Science ®Google Scholar
• Tomasson G, Grayson PC, Mahr AD, et al. Value of ANCA measurements during remission to predict a relapse of ANCA-associated vasculitis–a meta-analysis. Rheumatology (Oxford). 2012;51:100–109.
   PubMed Web of Science ®Google Scholar
• Fussner LA, Hummel AM, Schroeder DR, et al. Factors determining the clinical utility of serial measurements of antineutrophil cytoplasmic antibodies targeting proteinase 3. Arthritis Rheumatol. 2016;68:1700–1710.
   PubMed Web of Science ®Google Scholar
• Kemna MJ, Damoiseaux J, Austen J, et al. ANCA as a predictor of relapse: useful in patients with renal involvement but not in patients with nonrenal disease. JASN. 2015;26:537–542.
   Web of Science ®Google Scholar
• Cartin-Ceba R, Golbin JM, Keogh KA, et al. Rituximab for remission induction and maintenance in refractory granulomatosis with polyangiitis (Wegener’s): ten-year experience at a single center. Arthritis Rheumatol. 2012;64:3770–3778.
   PubMed Web of Science ®Google Scholar
• Rhee EP, Laliberte KA, Niles JL. Rituximab as maintenance therapy for anti-neutrophil cytoplasmic antibody-associated vasculitis. CJASN. 2010;5:1394–1400.
   PubMed Web of Science ®Google Scholar
• Smith RM, Jones RB, Guerry MJ, et al. Rituximab for remission maintenance in relapsing antineutrophil cytoplasmic antibody-associated vasculitis. Arthritis Rheumatol. 2012;64:3760–3769.
   PubMed Web of Science ®Google Scholar
• Guillevin L, Pagnoux C, Karras A, et al. Rituximab versus azathioprine for maintenance in ANCA-associated vasculitis. N Engl J Med. 2014;371:1771–1780.
   PubMed Web of Science ®Google Scholar
• Pendergraft WF 3rd, Cortazar FB, Wenger J, et al. Long-term maintenance therapy using rituximab-induced continuous B-cell depletion in patients with ANCA vasculitis. CJASN. 2014;9:736–744.
   PubMed Web of Science ®Google Scholar
• Timlin H, Lee SM, Manno RL, et al. Rituximab for remission induction in elderly patients with ANCA-associated vasculitis. Semin Arthritis Rheum. 2015;45:67–69.
   PubMed Web of Science ®Google Scholar
• Cortazar FB, Pendergraft WF 3rd, Wenger J, et al. The effect of continuous B cell depletion with rituximab on pathogenic autoantibodies and total IgG levels in ANCA vasculitis. Arthritis Rheumatol. 2017;69:1045–1053.
   PubMed Web of Science ®Google Scholar
• Alberici F, Smith RM, Jones RB, et al. Long-term follow-up of patients who received repeat-dose rituximab as maintenance therapy for ANCA-associated vasculitis. Rheumatology (Oxford). 2015;54:1153–1160.
   PubMed Web of Science ®Google Scholar
• Besada E, Koldingsnes W, Nossent JC. Long-term efficacy and safety of pre-emptive maintenance therapy with rituximab in granulomatosis with polyangiitis: results from a single centre. Rheumatology (Oxford). 2013;52:2041–2047.
   PubMed Web of Science ®Google Scholar
• Calich AL, Puechal X, Pugnet G, et al. Rituximab for induction and maintenance therapy in granulomatosis with polyangiitis (Wegener’s). Results of a single-center cohort study on 66 patients. J Autoimmun. 2014;50:135–141.
   PubMed Web of Science ®Google Scholar
• Charles P, Neel A, Tieulie N, et al. Rituximab for induction and maintenance treatment of ANCA-associated vasculitides: a multicentre retrospective study on 80 patients. Rheumatology (Oxford). 2014;53:532–539.
   PubMed Web of Science ®Google Scholar
• Mansfield N, Hamour S, Habib AM, et al. Prolonged disease-free remission following rituximab and low-dose cyclophosphamide therapy for renal ANCA-associated vasculitis. NTD. 2011;26:3280–3286.
   PubMed Web of Science ®Google Scholar
• Azar L, Springer J, Langford CA, et al. Rituximab with or without a conventional maintenance agent in the treatment of relapsing granulomatosis with polyangiitis (Wegener’s): a retrospective single-center study. Arthritis Rheumatol. 2014;66(10):2862–2870.
   PubMed Web of Science ®Google Scholar
• Puéchal X, Iudici M, Calich AL, et al. Rituximab for induction and maintenance therapy of granulomatosis with polyangiitis: a single-centre cohort study on 114 patients. Rheumatology (Oxford). 2019;58:401–409.
   PubMed Web of Science ®Google Scholar
• Pugnet G, Pagnoux C, Terrier B, et al. Rituximab versus azathioprine for ANCA-associated vasculitis maintenance therapy: impact on global disability and health-related quality of life. Clin Exp Rheumatol. 2016;34:S54–9.
   PubMed Web of Science ®Google Scholar
• Montante A, Le Bras A, Pagnoux C, et al. Cost-effectiveness of rituximab versus azathioprine for maintenance treatment in antineutrophil cytoplasmic antibody-associated vasculitis. Clin Exp Rheumatol. 2019;37:137–143.
   PubMed Web of Science ®Google Scholar
• Jones RB, Furuta S, Tervaert JW, et al. Rituximab versus cyclophosphamide in ANCA-associated renal vasculitis: 2-year results of a randomised trial. Ann Rheum Dis. 2015;74:1178–1182.
   PubMed Web of Science ®Google Scholar
• Besada E. Low immunoglobulin levels increase the risk of severe hypogammaglobulinemia in granulomatosis with polyangiitis patients receiving rituximab. BMC Musculoskelet Disord. 2016;17:6.
   PubMed Web of Science ®Google Scholar
• Roberts DM, Jones RB, Smith RM, et al. Rituximab-associated hypogammaglobulinemia: incidence, predictors and outcomes in patients with multi-system autoimmune disease. J Autoimmun. 2015;57:60–65.
   PubMed Web of Science ®Google Scholar
• Kronbichler A, Kerschbaum J, Gopaluni S, et al. Trimethoprim-sulfamethoxazole prophylaxis prevents severe/life-threatening infections following rituximab in antineutrophil cytoplasm antibody-associated vasculitis. Ann Rheumatic Dis. 2018;77:1440–1447.
   PubMed Web of Science ®Google Scholar
• Charles P, Terrier B, Perrodeau E, et al. Comparison of individually tailored versus fixed-schedule rituximab regimen to maintain ANCA-associated vasculitis remission: results of a multicentre, randomised controlled, phase III trial (MAINRITSAN2). Ann Rheum Dis. 2018;77:1143–1149.
   PubMed Web of Science ®Google Scholar
• Gopaluni S, Smith RM, Lewin M, et al. Rituximab versus azathioprine as therapy for maintenance of remission for anti-neutrophil cytoplasm antibody-associated vasculitis (RITAZAREM): study protocol for a randomized controlled trial. Trials. 2017;18:112.
   PubMed Web of Science ®Google Scholar
• Jayne D, Blockmans D, Luqmani R, et al. Efficacy and safety of belimumab and azathioprine for maintenance of remission in ANCA-associated vasculitis: A randomized controlled study. Arthritis Rheumatol. 2019;71:952–963.
   PubMed Web of Science ®Google Scholar
• Walsh M, Merkel PA, Mahr A, et al. Effects of duration of glucocorticoid therapy on relapse rate in antineutrophil cytoplasmic antibody-associated vasculitis: A meta-analysis. Arthritis Care Res (Hoboken). 2010;62:1166–1173.
   PubMed Web of Science ®Google Scholar
• Jayne DRW, Bruchfeld AN, Harper L, et al. Randomized trial of C5a receptor inhibitor Avacopan in ANCA-associated vasculitis. JASN. 2017;28:2756–2767.
   Web of Science ®Google Scholar
• Popa ER, Stegeman CA, Bos NA, et al. Differential B- and T-cell activation in Wegener’s granulomatosis. J Allergy Clin Immunol. 1999;103:885–894.
   PubMed Web of Science ®Google Scholar
• Abdulahad WH, Stegeman CA, Limburg PC, et al. Skewed distribution of Th17 lymphocytes in patients with Wegener’s granulomatosis in remission. Arthritis Rheumatol. 2008;58:2196–2205.
   PubMed Web of Science ®Google Scholar
• Langford CA, Monach PA, Specks U, et al. An open-label trial of abatacept (CTLA4-IG) in non-severe relapsing granulomatosis with polyangiitis (Wegener’s). Ann Rheum Dis. 2014;73:1376–1379.
   PubMed Web of Science ®Google Scholar