ANCA-associated vasculitis-clinical utility of using ANCA specificity to classify patients

Nature Reviews Rheumatology

Volumn 12, Issue 10, 2016, Pages 570-579

  Cornec, Divi ^a,b   Gall, Emilie Cornec Le ^a,b   Fervenza, Fernando C ^a   Specks, Ulrich ^a  

^a MAYO CLINIC   (United States)

^b UNIVERSITÉ EUROPÉENNE DE BRETAGNE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

AZATHIOPRINE; BACTERICIDAL PERMEABILITY INCREASING PROTEIN; CATHEPSIN G; CYCLOPHOSPHAMIDE; HLA DP ANTIGEN; LACTOFERRIN; LEUKOCYTE ELASTASE; METHOTREXATE; MYELOBLASTIN; MYELOPEROXIDASE; NEUTROPHIL CYTOPLASMIC ANTIBODY; PREDNISONE; RITUXIMAB; BIOLOGICAL MARKER; IMMUNOLOGIC FACTOR; PEROXIDASE;

ANCA ASSOCIATED VASCULITIS; ANTIBODY SPECIFICITY; COHORT ANALYSIS; DISEASE ASSOCIATION; DRUG EFFICACY; EOSINOPHILIC GRANULOMATOSIS WITH POLYANGIITIS; GENE; GENETIC ASSOCIATION; GENETIC PREDISPOSITION; HLADP GENE; HUMAN; IMMUNOFLUORESCENCE; IN VITRO STUDY; MICROSCOPIC POLYANGIITIS; MORTALITY; MULTICENTER STUDY (TOPIC); NONHUMAN; PATHOGENICITY; PHENOTYPE; PRIORITY JOURNAL; PRTN3 GENE; RANDOMIZED CONTROLLED TRIAL (TOPIC); REMISSION; REVIEW; SERPINA1 GENE; TREATMENT OUTCOME; TREATMENT RESPONSE; WEGENER GRANULOMATOSIS; ANTI-NEUTROPHIL CYTOPLASMIC ANTIBODY-ASSOCIATED VASCULITIS; BLOOD; CHURG-STRAUSS SYNDROME; CLASSIFICATION; GRANULOMATOSIS WITH POLYANGIITIS; IMMUNOLOGY; INFLAMMATION; PREDICTIVE VALUE; PROGNOSIS; SENSITIVITY AND SPECIFICITY;

ANTI-NEUTROPHIL CYTOPLASMIC ANTIBODY-ASSOCIATED VASCULITIS; ANTIBODIES, ANTINEUTROPHIL CYTOPLASMIC; BIOMARKERS; CHURG-STRAUSS SYNDROME; GRANULOMATOSIS WITH POLYANGIITIS; HUMANS; IMMUNOLOGIC FACTORS; INFLAMMATION; MICROSCOPIC POLYANGIITIS; MYELOBLASTIN; PEROXIDASE; PREDICTIVE VALUE OF TESTS; PROGNOSIS; SENSITIVITY AND SPECIFICITY;

EID: 84980002615     PISSN: 17594790     EISSN: 17594804     Source Type: Journal    
DOI: 10.1038/nrrheum.2016.123     Document Type: Review

References (156)

1. Davies, D. J., Moran, J. E., Niall, J. F., & Ryan, G. B. Segmental necrotising glomerulonephritis with antineutrophil antibody: possible arbovirus aetiology? Br. Med. J. (Clin. Res. Ed.) 285, 606 (1982).
2. Hall, J. B., Wadham, B. M., Wood, C. J., Ashton, V., & Adam, W. R. Vasculitis and glomerulonephritis: a subgroup with an antineutrophil cytoplasmic antibody. Aust. N. Z. J. Med. 14, 277-278 (1984).
3. van der Woude, F. J., et al. Autoantibodies against neutrophils and monocytes: tool for diagnosis and marker of disease activity in Wegener?s granulomatosis. Lancet 1, 425-429 (1985).
4. Falk, R. J., & Jennette, J. C. Anti-neutrophil cytoplasmic autoantibodies with specificity for myeloperoxidase in patients with systemic vasculitis and idiopathic necrotizing and crescentic glomerulonephritis. N. Engl. J. Med. 318, 1651-1657 (1988).
5. Ludemann, J., Utecht, B., & Gross, W. L. Anti-neutrophil cytoplasm antibodies in Wegener?s granulomatosis recognize an elastinolytic enzyme. J. Exp. Med. 171, 357-362 (1990).
6. Jenne, D. E., Tschopp, J., Ludemann, J., Utecht, B., & Gross, W. L. Wegener?s autoantigen decoded. Nature 346, 520 (1990).
7. Jennette, J. C., et al. 2012 revised International Chapel Hill Consensus Conference Nomenclature of Vasculitides. Arthritis Rheum. 65 1-11 2013).
8. Mahr, A., Guillevin, L., Poissonnet, M., & Ayme, S. Prevalences of polyarteritis nodosa, microscopic polyangiitis, Wegener?s granulomatosis, and Churg-Strauss syndrome in a French urban multiethnic population in 2000: a capture-recapture estimate. Arthritis Rheum. 51, 92-99 (2004).
9. Watts, R. A., et al. Classification, epidemiology and clinical subgrouping of antineutrophil cytoplasmic antibody (ANCA)-Associated vasculitis. Nephrol. Dial. Transplant. 30 (Suppl. 1), 14-22 (2015).
10. Groh, M., et al. Eosinophilic granulomatosis with polyangiitis (Churg-Strauss) (EGPA) Consensus Task Force recommendations for evaluation and management. Eur. J. Intern. Med. 26, 545-553 (2015).
11. Mukhtyar, C., et al. EULAR recommendations for the management of primary small and medium vessel vasculitis. Ann. Rheum. Dis. 68, 310-317 (2009).
12. Yates M., et al. EULAR/ERA-EDTA recommendations for the management of ANCA-Associated vasculitis. Ann. Rheum. Dis. http://dx.doi.org/10.1136/annrheumdis 2016 209133 2016).
13. Hunder, G. G., et al. The American College of Rheumatology 1990 criteria for the classification of vasculitis. Introduction. Arthritis Rheum. 33, 1065-1067 (1990).
14. Leavitt, R. Y., et al. The American College of Rheumatology 1990 criteria for the classification of Wegener?s granulomatosis. Arthritis Rheum. 33, 1101-1107 (1990).
15. Masi, A. T., et al. The American College of Rheumatology 1990 criteria for the classification of Churg-Strauss syndrome (allergic granulomatosis and angiitis). Arthritis Rheum. 33, 1094-1100 (1990).
16. Lightfoot, R. W. Jr., et al. The American College of Rheumatology 1990 criteria for the classification of polyarteritis nodosa. Arthritis Rheum. 33, 1088-1093 (1990).
17. Jennette, J. C., et al. Nomenclature of systemic vasculitides. Proposal of an international consensus conference. Arthritis Rheum. 37, 187-192 (1994).
18. Watts, R., et al. Development and validation of a consensus methodology for the classification of the ANCA-Associated vasculitides and polyarteritis nodosa for epidemiological studies. Ann. Rheum. Dis. 66, 222-227 (2007).
19. Watts, R. A., & Scott, D. G. ANCA vasculitis: to lump or split? Why we should study MPA and GPA separately. Rheumatology (Oxford) 51, 2115-2117 (2012).
20. Millet, A., Pederzoli-Ribeil, M., Guillevin, L., Witko-Sarsat, V., & Mouthon, L. Antineutrophil cytoplasmic antibody-Associated vasculitides: is it time to split up the group? Ann. Rheum. Dis. 72, 1273-1279 (2013).
21. Hilhorst, M., van Paassen, P., & Tervaert, J. W. Proteinase 3 ANCA vasculitis versus myeloperoxidase-ANCA vasculitis. J. Am. Soc. Nephrol. 26, 2314-2327 (2015).
22. Kallenberg, C. G. Key advances in the clinical approach to ANCA-Associated vasculitis. Nat. Rev. Rheumatol. 10, 484-493 (2014).
23. Lionaki, S., 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 Rheum. 64, 3452-3462 (2012).
24. Hagen, E. C., et al. Diagnostic value of standardized assays for anti-neutrophil cytoplasmic antibodies in idiopathic systemic vasculitis. EC/BCR project for ANCA assay standardization. Kidney Int. 53, 743-753 (1998).
25. Shah, S., Havill, J., Rahman, M. H., & Geetha, D. A historical study of American patients with anti-neutrophil cytoplasmic antibody negative pauci-immune glomerulonephritis. Clin. Rheumatol. 35, 953-960 (2016).
26. Yazici, H., & Yazici, Y. Diagnosis and/or classification of vasculitis: different? Curr. Opin. Rheumatol. 28, 3-7 (2016).
27. Craven, A., et al. ACR/EULAR-endorsed study to develop Diagnostic and Classification Criteria for Vasculitis (DCVAS). Clin. Exp. Nephrol. 17, 619-621 (2013).
28. Basu, N., et al. EULAR points to consider in the development of classification and diagnostic criteria in systemic vasculitis. Ann. Rheum. Dis. 69, 1744-1750 (2010).
29. Kallenberg, C. G. Usefulness of antineutrophil cytoplasmic autoantibodies in diagnosing and managing systemic vasculitis. Curr. Opin. Rheumatol. 28, 8-14 (2016).
30. Merkel, P. A., Polisson, R. P., Chang, Y., Skates, S. J., & Niles, J. L. Prevalence of antineutrophil cytoplasmic antibodies in a large inception cohort of patients with connective tissue disease. Ann. Intern. Med. 126, 866-873 (1997).
31. van der Geld, Y. M., Limburg, P. C., & Kallenberg, C. G. Proteinase 3, Wegener?s autoantigen: from gene to antigen. J. Leukoc. Biol. 69, 177-190 (2001).
32. Korkmaz, B., et al. Inhibitors and antibody fragments as potential anti-inflammatory therapeutics targeting neutrophil proteinase 3 in human disease. Pharmacol. Rev. 68, 603-630 (2016).
33. Capizzi, S. A., Viss, M. A., Hummel, A. M., Fass, D. N., & Specks, U. Effects of carboxy-Terminal modifications of proteinase 3 (PR3) on the recognition by PR3 ANCA. Kidney Int. 63, 756-760 (2003).
34. Witko-Sarsat, V., et al. Presence of proteinase 3 in secretory vesicles: evidence of a novel, highly mobilizable intracellular pool distinct from azurophil granules. Blood 94, 2487-2496 (1999).
35. Kantari, C., et al. Proteinase 3, the Wegener autoantigen, is externalized during neutrophil apoptosis: evidence for a functional association with phospholipid scramblase 1 and interference with macrophage phagocytosis. Blood 110, 4086-4095 (2007).
36. Csernok, E., Schmitt, W. H., Ernst, M., Bainton, D. F., & Gross, W. L. Membrane surface proteinase 3 expression and intracytoplasmic immunoglobulin on neutrophils from patients with ANCA-Associated vasculitides. Adv. Exp. Med. Biol. 336, 45-50 (1993).
37. Witko-Sarsat, V., et al. A large subset of neutrophils expressing membrane proteinase 3 is a risk factor for vasculitis and rheumatoid arthritis. J. Am. Soc. Nephrol. 10, 1224-1233 (1999).
38. McInnis, E. A., et al. Dysregulation of autoantigen genes in ANCA-Associated vasculitis involves alternative transcripts and new protein synthesis. J. Am. Soc. Nephrol. 26, 390-399 (2015).
39. Kessenbrock, K., et al. Netting neutrophils in autoimmune small-vessel vasculitis. Nat. Med. 15, 623-625 (2009).
40. Millet, A., et al. Proteinase 3 on apoptotic cells disrupts immune silencing in autoimmune vasculitis. J. Clin. Invest. 125, 4107-4121 (2015).
41. Kelley, J. M., et al. IgA and IgG antineutrophil cytoplasmic antibody engagement of Fc receptor genetic variants influences granulomatosis with polyangiitis. Proc. Natl Acad. Sci. USA 108, 20736-20741 (2011).
42. van der Veen, B. S., de Winther, M. P., & Heeringa, P. Myeloperoxidase: molecular mechanisms of action and their relevance to human health and disease. Antioxid. Redox. Signal. 11, 2899-2937 (2009).
43. Hess, C., Sadallah, S., & Schifferli, J. A. Induction of neutrophil responsiveness to myeloperoxidase antibodies by their exposure to supernatant of degranulated autologous neutrophils. Blood 96, 2822-2827 (2000).
44. O?Sullivan, K. M., et al. Renal participation of myeloperoxidase in antineutrophil cytoplasmic antibody (ANCA)-Associated glomerulonephritis. Kidney Int. 88, 1030-1046 (2015).
45. Coppo, R., et al. Properties of circulating IgA molecules in Henoch-Schonlein purpura nephritis with focus on neutrophil cytoplasmic antigen IgA binding (IgA-ANCA): new insight into a debated issue. Italian Group of Renal Immunopathology Collaborative Study on Henoch-Schonlein purpura in adults and in children. Nephrol. Dial. Transplant. 12, 2269-2276 (1997).
46. Bollee, G., et al. Pauci-immune crescentic glomerulonephritis associated with ANCA of IgA class. Am. J. Kidney Dis. 53, 1063-1067 (2009).
47. Talor, M. V., et al. Antibodies to selected minor target antigens in patients with anti-neutrophil cytoplasmic antibodies (ANCA). Clin. Exp. Immunol. 150, 42-48 (2007).
48. Kida, I., et al. Antineutrophil cytoplasmic antibodies against myeloperoxidase, proteinase 3, elastase, cathepsin G and lactoferrin in Japanese patients with rheumatoid arthritis. Mod. Rheumatol. 21, 43-50 (2011).
49. Khanna, D., Aggarwal, A., Bhakuni, D. S., Dayal, R., & Misra, R. Bactericidal/permeability-increasing protein and cathepsin G are the major antigenic targets of antineutrophil cytoplasmic autoantibodies in systemic sclerosis. J. Rheumatol. 30, 1248-1252 (2003).
50. Teixeira, L., et al. Low seroprevalence and poor specificity of antineutrophil cytoplasmic antibodies in tuberculosis. Rheumatology (Oxford) 44, 247-250 (2005).
51. Cornely, O. A., et al. Seroprevalence and disease association of antineutrophil cytoplasmic autoantibodies and antigens in HIV infection. Infection 27, 92-96 (1999).
52. Mahr, A., et al. Brief report: prevalence of antineutrophil cytoplasmic antibodies in infective endocarditis. Arthritis Rheumatol. 66, 1672-1677 (2014).
53. Bonneau, J., et al. Systematic review: new serological markers (anti-glycan, anti GP2, anti GM CSF Ab) in the prediction of IBD patient outcomes. Autoimmun. Rev. 14, 231-245 (2015).
54. Wiesner, O., et al. Antineutrophil cytoplasmic antibodies reacting with human neutrophil elastase as a diagnostic marker for cocaine-induced midline destructive lesions but not autoimmune vasculitis. Arthritis Rheum. 50, 2954-2965 (2004).
55. Peikert, T., et al. Functional characterization of antineutrophil cytoplasmic antibodies in patients with cocaine-induced midline destructive lesions. Arthritis Rheum. 58, 1546-1551 (2008).
56. Kain, R., et al. A novel class of autoantigens of anti-neutrophil cytoplasmic antibodies in necrotizing and crescentic glomerulonephritis: the lysosomal membrane glycoprotein h lamp 2 in neutrophil granulocytes and a related membrane protein in glomerular endothelial cells. J. Exp. Med. 181, 585-597 (1995).
57. Kain, R., et al. Molecular mimicry in pauci-immune focal necrotizing glomerulonephritis. Nat. Med. 14, 1088-1096 (2008).
58. Kain, R., et al. High prevalence of autoantibodies to hLAMP 2 in anti-neutrophil cytoplasmic antibody-Associated vasculitis. J. Am. Soc. Nephrol. 23, 556-566 (2012).
59. Roth, A. J., et al. Anti-LAMP 2 antibodies are not prevalent in patients with antineutrophil cytoplasmic autoantibody glomerulonephritis. J. Am. Soc. Nephrol. 23, 545-555 (2012).
60. Fervenza, F. C., & Specks, U. Vasculitis: Will LAMP enlighten us about ANCA-Associated vasculitis? Nat. Rev. Nephrol. 8, 318-320 (2012).
61. Land, J., Rutgers, A., & Kallenberg, C. G. Anti-neutrophil cytoplasmic autoantibody pathogenicity revisited: pathogenic versus non-pathogenic anti-neutrophil cytoplasmic autoantibody. Nephrol. Dial. Transplant. 29, 739-745 (2014).
62. Jennette, J. C., & Falk, R. J. Pathogenesis of antineutrophil cytoplasmic autoantibody-mediated disease. Nat. Rev. Rheumatol. 10, 463-473 (2014).
63. Xiao H., et al. Antineutrophil cytoplasmic autoantibodies specific for myeloperoxidase cause glomerulonephritis and vasculitis in mice. J. Clin. Invest.110, 955-963 2002).
64. Little, M. A., et al. Antineutrophil cytoplasm antibodies directed against myeloperoxidase augment leukocyte-microvascular interactions in vivo. Blood 106, 2050-2058 (2005).
65. Korkmaz, B., Jenne, D. E., & Gauthier, F. Relevance of the mouse model as a therapeutic approach for neutrophil proteinase 3 associated human diseases. Int. Immunopharmacol. 17, 1198-1205 (2013).
66. Wiesner, O., et al. Differences between human proteinase 3 and neutrophil elastase and their murine homologues are relevant for murine model experiments. FEBS Lett. 579, 5305-5312 (2005).
67. Falk, R. J., Terrell, R. S., Charles, L. A., & Jennette, J. C. Anti-neutrophil cytoplasmic autoantibodies induce neutrophils to degranulate and produce oxygen radicals in vitro. Proc. Natl Acad. Sci. USA 87, 4115-4119 (1990).
68. Harper, L., et al. IgG from myeloperoxidase-Antineutrophil cytoplasmic antibody-positive patients stimulates greater activation of primed neutrophils than IgG from proteinase 3 antineutrophil cytosplasmic antibody-positive patients. Arthritis Rheum. 44, 921-930 (2001).
69. Espy, C., et al. Sialylation levels of anti-proteinase 3 antibodies are associated with the activity of granulomatosis with polyangiitis (Wegener?s). Arthritis Rheum. 63, 2105-2115 (2011).
70. Wuhrer, M., et al. Skewed Fc glycosylation profiles of anti-proteinase 3 immunoglobulin G1 autoantibodies from granulomatosis with polyangiitis patients show low levels of bisection, galactosylation, and sialylation. J. Proteome Res. 14, 1657-1665 (2015).
71. Bansal, P. J., & Tobin, M. C. Neonatal microscopic polyangiitis secondary to transfer of maternal myeloperoxidase-Antineutrophil cytoplasmic antibody resulting in neonatal pulmonary hemorrhage and renal involvement. Ann. Allergy Asthma Immunol. 93, 398-401 (2004).
72. Silva, F., Specks, U., Sethi, S., Irazabal, M. V., & Fervenza, F. C. Successful pregnancy and delivery of a healthy newborn despite transplacental transfer of antimyeloperoxidase antibodies from a mother with microscopic polyangiitis. Am. J. Kidney Dis. 54, 542-545 (2009).
73. Finkielman, J. D., et al. ANCA are detectable in nearly all patients with active severe Wegener?s granulomatosis. Am. J. Med. 120, 643.e9-643.e14 (2007).
74. Cui, Z., Zhao, M. H., Segelmark, M., & Hellmark, T. Natural autoantibodies to myeloperoxidase, proteinase 3, and the glomerular basement membrane are present in normal individuals. Kidney Int. 78, 590-597 (2010).
75. Roth, A. J., et al. Epitope specificity determines pathogenicity and detectability in ANCA-Associated vasculitis. J. Clin. Invest. 123, 1773-1783 (2013).
76. Silva, F., Hummel, A. M., Jenne, D. E., & Specks, U. Discrimination and variable impact of ANCA binding to different surface epitopes on proteinase 3, the Wegener?s autoantigen. J. Autoimmun. 35, 299-308 (2010).
77. Glasner, C., et al. Low anti-staphylococcal IgG responses in granulomatosis with polyangiitis patients despite long-Term Staphylococcus aureus exposure. Sci. Rep. 5, 8188 (2015).
78. Pendergraft, W. F., 3rd et al. Autoimmunity is triggered by cPR 3(105-201), a protein complementary to human autoantigen proteinase 3. Nat. Med. 10, 72-79 (2004).
79. Tadema, H., Kallenberg, C. G., Stegeman, C. A., & Heeringa, P. Reactivity against complementary proteinase 3 is not increased in patients with PR3 ANCA-Associated vasculitis. PLoS ONE 6, e17972 (2011).
80. Preston, G., & Falk, R. Autoimmunity: does autoantigen complementarity underlie PR3 ANCA AAV? Nat. Rev. Rheumatol. 7, 439-440 (2011).
81. Spencer, S. J., Burns, A., Gaskin, G., Pusey, C. D., & Rees, A. J. HLA class II specificities in vasculitis with antibodies to neutrophil cytoplasmic antigens. Kidney Int. 41, 1059-1063 (1992).
82. Mahr, A. D., et al. Alpha1-Antitrypsin deficiency-related alleles Z and S and the risk of Wegener?s granulomatosis. Arthritis Rheum. 62, 3760-3767 (2010).
83. Chung, S. A., et al. Meta-Analysis of genetic polymorphisms in granulomatosis with polyangiitis (Wegener?s) reveals shared susceptibility loci with rheumatoid arthritis. Arthritis Rheum. 64, 3463-3471 (2012).
84. Xie, G., et al. Association of granulomatosis with polyangiitis (Wegener?s) with HLA DPB104 and SEMA6A gene variants: evidence from genome-wide analysis. Arthritis Rheum. 65, 2457-2468 (2013).
85. Wieczorek, S., et al. The SEM6A6 locus is not associated with granulomatosis with polyangiitis or other forms of antineutrophil cytoplasmic antibody-Associated vasculitides in Europeans: comment on the article by Xie et al. Arthritis Rheumatol. 66, 1400-1401 (2014).
86. Farrer, L. A., Sherva, R., Merkel, P. A., & Siminovitch, K. A. Reply: to PMID 23740775. Arthritis Rheumatol. 66, 1401 (2014).
87. Lyons, P. A., et al. Genetically distinct subsets within ANCA-Associated vasculitis. N. Engl. J. Med. 367, 214-223 (2012).
88. Rahmattulla C., et al. Genetic variants in ANCA-Associated vasculitis: a meta-Analysis. Ann. Rheum. Dis. http://dx.doi.org/10.1136/annrheumdis 2015 207601 2015).
89. Herlyn, K., Buckert, F., Gross, W. L., & Reinhold-Keller, E. Doubled prevalence rates of ANCA-Associated vasculitides and giant cell arteritis between 1994 and 2006 in northern Germany. Rheumatology (Oxford) 53, 882-889 (2014).
90. Knight, A., Ekbom, A., Brandt, L., & Askling, J. Increasing incidence of Wegener?s granulomatosis in Sweden, 1975-2001. J. Rheumatol. 33, 2060-2063 (2006).
91. Fujimoto, S., et al. Comparison of the epidemiology of anti-neutrophil cytoplasmic antibody-Associated vasculitis between Japan and the UK. Rheumatology (Oxford) 50, 1916-1920 (2011).
92. Sada, K. E., et al. Classification and characteristics of Japanese patients with antineutrophil cytoplasmic antibody-Associated vasculitis in a nationwide, prospective, inception cohort study. Arthritis Res. Ther. 16, R101 (2014).
93. Comarmond, C., et al. Pulmonary fibrosis in antineutrophil cytoplasmic antibodies (ANCA)-Associated vasculitis: a series of 49 patients and review of the literature. Med. (Baltimore) 93, 340-349 (2014).
94. Cartin-Ceba, R., et al. Diffuse alveolar hemorrhage secondary to ANCA-Associated vasculitis: predictors of respiratory failure and clinical outcomes. Arthritis Rheumatol. 68, 1467-1476 (2016).
95. Franssen, C. F., et al. Antiproteinase 3-And antimyeloperoxidase-Associated vasculitis. Kidney Int. 57, 2195-2206 (2000).
96. Stone, J. H., et al. Rituximab versus cyclophosphamide for ANCA-Associated vasculitis. N. Engl. J. Med. 363, 221-232 (2010).
97. Unizony, S., et al. Clinical outcomes of treatment of anti-neutrophil cytoplasmic antibody (ANCA)-Associated vasculitis based on ANCA type. Ann. Rheum. Dis. 75, 1166-1169 (2016).
98. Geetha, D., et al. Rituximab versus cyclophosphamide for ANCA-Associated vasculitis with renal involvement. J. Am. Soc. Nephrol. 26, 976-985 (2015).
99. Brockmann, H., et al. Proteinase 3 as the major autoantigen of c ANCA is strongly expressed in lung tissue of patients with Wegener?s granulomatosis. Arthritis Res. 4, 220-225 (2002).
100. Schwarting, A., et al. Proteinase 3 mRNA expressed by glomerular epithelial cells correlates with crescent formation in Wegener?s granulomatosis. Kidney Int. 57, 2412-2422 (2000).
101. Schirmer, J. H., et al. Myeloperoxidase-ANCA associated Granulomatosis with polyangiitis is a clinically distinct subset within ANCA-Associated vasculitis. Arthritis Rheumatol. http://dx.doi. org/10.1002/art.39786 (2016).
102. Mahr, A., et al. Revisiting the classification of clinical phenotypes of anti-neutrophil cytoplasmic antibody-Associated vasculitis: a cluster analysis. Ann. Rheum. Dis. 72, 1003-1010 (2013).
103. Csernok, E., Ahlquist, D., Ullrich, S., & Gross, W. L. A critical evaluation of commercial immunoassays for antineutrophil cytoplasmic antibodies directed against proteinase 3 and myeloperoxidase in Wegener?s granulomatosis and microscopic polyangiitis. Rheumatology (Oxford) 41, 1313-1317 (2002).
104. Chen, M., Kallenberg, C. G., & Zhao, M. H. ANCA-negative pauci-immune crescentic glomerulonephritis. Nat. Rev. Nephrol. 5, 313-318 (2009).
105. Stone, J. H. Limited versus severe Wegener?s granulomatosis: baseline data on patients in the Wegener?s granulomatosis etanercept trial. Arthritis Rheum. 48, 2299-2309 (2003).
106. Holle, J. U., et al. Prospective long-Term follow up of patients with localised Wegener?s granulomatosis: does it occur as persistent disease stage? Ann. Rheum. Dis. 69, 1934-1939 (2010).
107. Mouthon, L., Dunogue, B., & Guillevin, L. Diagnosis and classification of eosinophilic granulomatosis with polyangiitis (formerly named Churg-Strauss syndrome). J. Autoimmun. 48-49, 99-103 (2014).
108. Sable-Fourtassou, R., et al. Antineutrophil cytoplasmic antibodies and the Churg-Strauss syndrome. Ann. Intern. Med. 143, 632-638 (2005).
109. Comarmond, C., et al. Eosinophilic granulomatosis with polyangiitis (Churg-Strauss): clinical characteristics and long-Term followup of the 383 patients enrolled in the French Vasculitis Study Group cohort. Arthritis Rheum. 65, 270-281 (2013).
110. Sokolowska, B. M., et al. ANCA-positive and ANCA-negative phenotypes of eosinophilic granulomatosis with polyangiitis (EGPA): outcome and long-Term follow up of 50 patients from a single Polish center. Clin. Exp. Rheumatol. 32 (Suppl. 82), S41-S47 (2014).
111. Durel, C. A., et al. Long-Term follow up of a multicentre cohort of 101 patients with eosinophilic granulomatosis with polyangiitis (EGPA). Arthritis Care Res. (Hoboken) 68, 374-387 (2016).
112. Groh, M., et al. Heart transplantation in patients with eosinophilic granulomatosis with polyangiitis (Churg-Strauss syndrome). J. Heart Lung Transplant. 33, 842-850 (2014).
113. Dunogue, B., et al. Impact of cardiac magnetic resonance imaging on eosinophilic granulomatosis with polyangiitis outcomes: A long-Term retrospective study on 42 patients. Autoimmun. Rev. 14, 774-780 (2015).
114. Guillevin, L., et al. A prospective, multicenter, randomized trial comparing steroids and pulse cyclophosphamide versus steroids and oral cyclophosphamide in the treatment of generalized Wegener?s granulomatosis. Arthritis Rheum. 40, 2187-2198 (1997).
115. Jayne, D., et al. A randomized trial of maintenance therapy for vasculitis associated with antineutrophil cytoplasmic autoantibodies. N. Engl. J. Med. 349, 36-44 (2003).
116. Hogan, S. L., et al. Predictors of relapse and treatment resistance in antineutrophil cytoplasmic antibody-Associated small-vessel vasculitis. Ann. Intern. Med. 143, 621-631 (2005).
117. De Groot, K., et al. Randomized trial of cyclophosphamide versus methotrexate for induction of remission in early systemic antineutrophil cytoplasmic antibody-Associated vasculitis. Arthritis Rheum. 52, 2461-2469 (2005).
118. Wegener?s Granulomatosis Etanercept Trial (WGET) Research Group. Etanercept plus standard therapy for Wegener?s granulomatosis. N. Engl. J. Med. 352, 351-361 (2005).
119. Pagnoux, C., et al. Azathioprine or methotrexate maintenance for ANCA-Associated vasculitis. N. Engl. J. Med. 359, 2790-2803 (2008).
120. de Groot, K., et al. Pulse versus daily oral cyclophosphamide for induction of remission in antineutrophil cytoplasmic antibody-Associated vasculitis: a randomized trial. Ann. Intern. Med. 150, 670-680 (2009).
121. Pagnoux, C., et al. Predictors of treatment resistance and relapse in antineutrophil cytoplasmic antibody-Associated small-vessel vasculitis: comparison of two independent cohorts. Arthritis Rheum. 58, 2908-2918 (2008).
122. Mohammad, A. J., et al. Rituximab for the treatment of eosinophilic granulomatosis with polyangiitis (Churg-Strauss). Ann. Rheum. Dis. 75, 396-401 (2016).
123. Puechal, X., et al. Long-Term outcomes of the WEGENT trial on remission-maintenance for granulomatosis with polyangiitis or microscopic polyangiitis. Arthritis Rheumatol. 68, 690-701 (2016).
124. Slot, M. C., Tervaert, J. W., Boomsma, M. M., & Stegeman, C. A. Positive classic antineutrophil cytoplasmic antibody (C ANCA) titer at switch to azathioprine therapy associated with relapse in proteinase 3 related vasculitis. Arthritis Rheum. 51, 269-273 (2004).
125. Sanders, J. F., 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. Nephrol. Dial. Transplant. http://dx.doi.org/10.1093/ndt/gfw211 (2016).
126. Hilhorst, M., et al. HLA DPB1 as a risk factor for relapse in antineutrophil cytoplasmic antibody-Associated vasculitis: a cohort study. Arthritis Rheumatol. 68, 1721-1730 (2016).
127. Fussner, L. A., & Specks, U. Can antineutrophil cytoplasmic antibody levels be used to inform treatment of pauci-immune vasculitis? Curr. Opin. Rheumatol. 27, 231-240 (2015).
128. Terrier, B., et al. Antimyeloperoxidase antibodies are a useful marker of disease activity in antineutrophil cytoplasmic antibody-Associated vasculitides. Ann. Rheum. Dis. 68, 1564-1571 (2009).
129. Finkielman, J. D., et al. Antiproteinase 3 antineutrophil cytoplasmic antibodies and disease activity in Wegener granulomatosis. Ann. Intern. Med. 147, 611-619 (2007).
130. Csernok, E., & Moosig, F. Current and emerging techniques for ANCA detection in vasculitis. Nat. Rev. Rheumatol. 10, 494-501 (2014).
131. Specks, U. Accurate relapse prediction in ANCA-Associated vasculitis-The search for the Holy Grail. J. Am. Soc. Nephrol. 26, 505-507 (2015).
132. Tomasson, G., Grayson, P. C., Mahr, A. D., Lavalley, M., & Merkel, P. A. Value of ANCA measurements during remission to predict a relapse of ANCA-Associated vasculitis a meta-Analysis. Rheumatology (Oxford) 51, 100-109 (2012).
133. Kemna, M. J., et al. ANCA as a predictor of relapse: useful in patients with renal involvement but not in patients with nonrenal disease. J. Am. Soc. Nephrol. 26, 537-542 (2015).
134. Fussner, L. A., et al. Factors determining the clinical utility of serial measurements of antineutrophil cytoplasmic antibodies targeting proteinase 3. Arthritis Rheumatol. 68, 1700-1710 (2016).
135. Guillevin, L., et al. Rituximab versus azathioprine for maintenance in ANCA-Associated vasculitis. N. Engl. J. Med. 371, 1771-1780 (2014).
136. Specks, U., et al. Efficacy of remission-induction regimens for ANCA-Associated vasculitis. N. Engl. J. Med. 369, 417-427 (2013).
137. Cartin-Ceba, R., et al. Rituximab for remission induction and maintenance in refractory granulomatosis with polyangiitis (Wegener?s): ten-year experience at a single center. Arthritis Rheum. 64, 3770-3778 (2012).
138. US National Library of Medicine. Comparison Study of Two Rituximab Regimens in the Remission of ANCA Associated Vasculitis (MAINRITSAN 2). ClinicalTrials.gov https://clinicaltrials.gov/ct2/show/NCT01731561 (2016).
139. Fauci, A. S., & Wolff, S. M. Wegener?s granulomatosis: studies in eighteen patients and a review of the literature. Med. (Baltimore) 52, 535-561 (1973).
140. Bhamra, K., & Luqmani, R. Damage assessment in ANCA-Associated vasculitis. Curr. Rheumatol. Rep. 14, 494-500 (2012).
141. Holle, J. U., et al. Improved outcome in 445 patients with Wegener?s granulomatosis in a German vasculitis center over four decades. Arthritis Rheum. 63, 257-266 (2011).
142. Hilhorst, M., et al. Improved outcome in anti-neutrophil cytoplasmic antibody (ANCA)-Associated glomerulonephritis: a 30 year follow up study. Nephrol. Dial. Transplant. 28, 373-379 (2013).
143. Rhee, R. L., et al. Trends in long-Term outcomes among patients with ANCA-Associated vasculitis with renal disease. Arthritis Rheumatol. 68, 1711-1720 (2016).
144. Flossmann, O., et al. Long-Term patient survival in ANCA-Associated vasculitis. Ann. Rheum. Dis. 70, 488-494 (2011).
145. de Joode, A. A., Sanders, J. S., & Stegeman, C. A. Renal survival in proteinase 3 and myeloperoxidase ANCA-Associated systemic vasculitis. Clin. J. Am. Soc. Nephrol. 8, 1709-1717 (2013).
146. Mohammad, A. J., & Segelmark, M. A population-based study showing better renal prognosis for proteinase 3 antineutrophil cytoplasmic antibody (ANCA)-Associated nephritis versus myeloperoxidase ANCA-Associated nephritis. J. Rheumatol. 41, 1366-1373 (2014).
147. Robson, J., 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) 54, 471-481 (2015).
148. Westman, K., Flossmann, O., & Gregorini, G. The long-Term outcomes of systemic vasculitis. Nephrol. Dial. Transplant. 30 (Suppl. 1), i60-i66 (2015).
149. Sada, K. E., et al. Different responses to treatment across classified diseases and severities in Japanese patients with microscopic polyangiitis and granulomatosis with polyangiitis: a nationwide prospective inception cohort study. Arthritis Res. Ther. 17, 305 (2015).
150. Tanna, A., et al. Long-Term outcome of anti-neutrophil cytoplasm antibody-Associated glomerulonephritis: evaluation of the international histological classification and other prognostic factors. Nephrol. Dial. Transplant. 30, 1185-1192 (2015).
151. Berden, A. E., et al. Histopathologic classification of ANCA-Associated glomerulonephritis. J. Am. Soc. Nephrol. 21, 1628-1636 (2010).
152. Rahmattulla, C., Bruijn, J. A., & Bajema, I. M. Histopathological classification of antineutrophil cytoplasmic antibody-Associated glomerulonephritis: an update. Curr. Opin. Nephrol. Hypertens. 23, 224-231 (2014).
153. Franssen, C. F., et al. Differences between anti-myeloperoxidase-And anti-proteinase 3 associated renal disease. Kidney Int. 47, 193-199 (1995).
154. Quintana, L. F., et al. ANCA serotype and histopathological classification for the prediction of renal outcome in ANCA-Associated glomerulonephritis. Nephrol. Dial. Transplant. 29, 1764-1769 (2014).
155. Guilpain, P., et al. Pathogenic effects of antimyeloperoxidase antibodies in patients with microscopic polyangiitis. Arthritis Rheum. 56, 2455-2463 (2007).
156. Watts, R. A., et al. Epidemiology of vasculitis in Europe. Ann. Rheum. Dis. 60, 1156-1157 (2001).