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Journal of Immunology Research
Volume 2014 (2014), Article ID 185416, 12 pages
http://dx.doi.org/10.1155/2014/185416
Review Article

Novel Clinical and Diagnostic Aspects of Antineutrophil Cytoplasmic Antibodies

1Department of Research, INOVA Diagnostics Inc., 9900 Old Grove Road, San Diego, CA 92131-1638, USA
2Microbiology and Virology Institute, San Carlo Borromeo Hospital, Via Pio II 3, 20153 Milan, Italy
3Division of Immunology, University Hospital Marqués de Valdecilla-IFIMAV, Avenida Valdecilla, 39008 Santander, Spain
4Department of Immunology and Internal Medicine, Hospital of Pitie-Salpêtriere, Boulevard de l’Hôpital, 75634 Paris, France
5Department of Medicine, University of Calgary, 3330 Hospital Dr. NW, Calgary, AB, Canada T2N 4N1

Received 4 February 2014; Accepted 6 March 2014; Published 5 June 2014

Academic Editor: Marvin J. Fritzler

Copyright © 2014 Johannes Schulte-Pelkum et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. A. Radice and R. A. Sinico, “Antineutrophil cytoplasmic antibodies (ANCA),” Autoimmunity, vol. 38, no. 1, pp. 93–103, 2005. View at Publisher · View at Google Scholar · View at Scopus
  2. D. J. Davies, J. E. Moran, J. F. Niall, and G. B. Ryan, “Segmental necrotising glomerulonephritis with antineutrophil antibody: possible arbovirus aetiology?” British Medical Journal, vol. 285, no. 6342, p. 606, 1982. View at Google Scholar · View at Scopus
  3. A. Wiik, “Delineation of a standard procedure for indirect immunofluorescence detection of ANCA,” APMIS, Supplement, vol. 97, no. 6, pp. 12–13, 1989. View at Google Scholar · View at Scopus
  4. F. J. van der Woude, N. Rasmussen, and S. Lobatto, “Autoantibodies against neutrophils and monocytes: tool for diagnosis and marker of disease activity in Wegener's granulomatosis,” The Lancet, vol. 1, no. 8426, pp. 425–429, 1985. View at Google Scholar · View at Scopus
  5. R. J. Falk and J. C. Jennette, “Anti-neutrophil cytoplasmic autoantibodies with specificity for myeloperoxidase in patients with systemic vasculitis and idiopathic necrotizing and crescentic glomerulonephritis,” The New England Journal of Medicine, vol. 318, no. 25, pp. 1651–1657, 1988. View at Google Scholar · View at Scopus
  6. J. L. Niles, R. T. McCluskey, M. F. Ahmad, and M. A. Arnaout, “Wegener's granulomatosis autoantigen is a novel neutrophil serine proteinase,” Blood, vol. 74, no. 6, pp. 1888–1893, 1989. View at Google Scholar · View at Scopus
  7. J. C. Jennette, A. S. Wilkman, and R. J. Falk, “Anti-neutrophil cytoplasmic autoantibody-associated glomerulonephritis and vasculitis,” American Journal of Pathology, vol. 135, no. 5, pp. 921–930, 1989. View at Google Scholar · View at Scopus
  8. R. Kain, K. Matsui, M. Exner 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,” Journal of Experimental Medicine, vol. 181, no. 2, pp. 585–597, 1995. View at Publisher · View at Google Scholar · View at Scopus
  9. M. V. Talor, J. H. Stone, J. Stebbing, J. Barin, N. R. Rose, and C. L. Burek, “Antibodies to selected minor target antigens in patients with anti-neutrophil cytoplasmic antibodies (ANCA),” Clinical and Experimental Immunology, vol. 150, no. 1, pp. 42–48, 2007. View at Publisher · View at Google Scholar · View at Scopus
  10. J. A. Savige, D. J. Davies, and P. A. Gatenby, “Anti-neutrophil cytoplasmic antibodies (ANCA): their detection and significance: report from workshops,” Pathology, vol. 26, no. 2, pp. 186–193, 1994. View at Google Scholar · View at Scopus
  11. A. Radice, L. Bianchi, and R. A. Sinico, “Anti-neutrophil cytoplasmic autoantibodies: methodological aspects and clinical significance in systemic vasculitis,” Autoimmunity Reviews, vol. 12, pp. 487–495, 2013. View at Google Scholar
  12. A. Radice, E. Sabadini, and A. Sinico, “Antineutrophil antibodies with specificity for Proteinase 3,” in Autoantibodies, Y. Shoenfeld, M. E. Gershwin, and P. L. Meroni, Eds., pp. 105–110, Elsevier, Oxford, UK, 2nd edition, 2007. View at Google Scholar
  13. C. Kallenberg, “Antineutrophil antibodies with specificity for Myeloperoxidase,” in Autoantibodies, Y. Shoenfeld, M. E. Gershwin, and P. L. Meroni, Eds., pp. 95–103, Elsevier, Oxford, UK, 2nd edition, 2007. View at Google Scholar
  14. P. Seo and J. H. Stone, “The antineutrophil cytoplasmic antibody-associated vasculitides,” American Journal of Medicine, vol. 117, no. 1, pp. 39–50, 2004. View at Publisher · View at Google Scholar · View at Scopus
  15. J. C. Jennette, R. J. Falk, P. A. Bacon et al., “2012 revised international Chapel Hill consensus Conference nomenclature of vasculitides,” Arthritis & Rheumatology, vol. 65, pp. 1–11, 2013. View at Google Scholar
  16. J. C. Jennette, R. J. Falk, P. Hu, and H. Xiao, “Pathogenesis of antineutrophil cytoplasmic autoantibody-associated small-vessel vasculitis,” Annual Review of Pathology, vol. 8, pp. 139–160, 2013. View at Google Scholar
  17. M. Mahler, A. Radice, W. Yang et al., “Development and performance evaluation of novel chemiluminescence assays for detection of anti-PR3 and anti-MPO antibodies,” Clinica Chimica Acta, vol. 413, no. 7-8, pp. 719–726, 2012. View at Publisher · View at Google Scholar · View at Scopus
  18. M. Mahler, A. Seaman, W. Yang, and G. Engstler, “Comparison of QUANTA Flash MPO with three other assays for the detection of MPO-ANCA,” in Proceedings of the International Congress on Controversies in Rheumatology and Autoimmunity (CORA '13), Budapest, Hungary, 2013.
  19. M. T. Arias-Loste, G. Bonilla, I. Moraleja et al., “Presence of anti-proteinase 3 antineutrophil cytoplasmic antibodies (anti-PR3 ANCA) as serologic markers in inflammatory bowel disease,” Clinical Reviews in Allergy & Immunology, vol. 45, no. 1, pp. 109–116, 2013. View at Google Scholar
  20. C. Roozendaal and C. G. M. Kallenberg, “Are anti-neutrophil cytoplasmic antibodies (ANCA) clinically useful in inflammatory bowel disease (IBD)?” Clinical and Experimental Immunology, vol. 116, no. 2, pp. 206–213, 1999. View at Publisher · View at Google Scholar · View at Scopus
  21. G. Deniziaut, E. Ballot, and C. Johanet, “Antineutrophil cytoplasmic auto-antibodies (ANCA) in autoimmune hepatitis and primary sclerosing cholangitis,” Clinics and Research in Hepatology and Gastroenterology, vol. 37, pp. 105–107, 2013. View at Google Scholar
  22. I. Lochman, V. Král, A. Lochmanová, J. LupaC, and L. Cebecauer, “ANCA in the diagnosis of neutrophil-mediated inflammation,” Autoimmunity Reviews, vol. 10, no. 6, pp. 295–298, 2011. View at Publisher · View at Google Scholar · View at Scopus
  23. J. Savige, D. Gillis, E. Benson et al., “International consensus statement on testing and reporting of antineutrophil cytoplasmic antibodies (ANCA),” American Journal of Clinical Pathology, vol. 111, no. 4, pp. 507–513, 1999. View at Google Scholar · View at Scopus
  24. M. Chen and C. G. M. Kallenberg, “New advances in the pathogenesis of ANCA-associated vasculitides,” Clinical and Experimental Rheumatology, vol. 27, no. 1, pp. S108–S114, 2009. View at Google Scholar · View at Scopus
  25. R. Kain, M. Exner, R. Brandes et al., “Molecular mimicry in pauci-immune focal necrotizing glomerulonephritis,” Nature Medicine, vol. 14, no. 10, pp. 1088–1096, 2008. View at Publisher · View at Google Scholar · View at Scopus
  26. A. J. Roth, M. C. Brown, R. N. Smith et al., “Anti-LAMP-2 antibodies are not prevalent in patients with antineutrophil cytoplasmic autoantibody glomerulonephritis,” Journal of the American Society of Nephrology, vol. 23, no. 3, pp. 545–555, 2012. View at Publisher · View at Google Scholar · View at Scopus
  27. K. Kessenbrock, M. Krumbholz, U. Schönermarck et al., “Netting neutrophils in autoimmune small-vessel vasculitis,” Nature Medicine, vol. 15, no. 6, pp. 623–625, 2009. View at Publisher · View at Google Scholar · View at Scopus
  28. V. Brinkmann, U. Reichard, C. Goosmann et al., “Neutrophil Extracellular Traps Kill Bacteria,” Science, vol. 303, no. 5663, pp. 1532–1535, 2004. View at Publisher · View at Google Scholar · View at Scopus
  29. M. J. Kaplan, “Neutrophils in the pathogenesis and manifestations of SLE,” Nature Reviews Rheumatology, vol. 7, no. 12, pp. 691–699, 2011. View at Publisher · View at Google Scholar · View at Scopus
  30. S. Sangaletti, C. Tripodo, C. Chiodoni et al., “Neutrophil extracellular traps mediate transfer of cytoplasmic neutrophil antigens to myeloid dendritic cells toward ANCA induction and associated autoimmunity,” Blood, vol. 120, pp. 3007–3018, 2012. View at Google Scholar
  31. K. Conrad, W. Schößler, F. Hiepe, and M. Fritzler, “Myeloperoxidase antibodies,” in Autoantibodies in Systemic Autoimmune Diseases—A Diagnostic Reference, K. Conrad, W. Schößler, F. Hiepe, and F. M. Pabst, Eds., pp. 111–113, 2nd edition, 2007. View at Google Scholar
  32. K. Conrad, W. Schößler, F. Hiepe, and M. Fritzler, “Proteinase 3 antibodies,” in Autoantibodies in Systemic Autoimmune Diseases—A Diagnostic Reference, K. Conrad, W. Schößler, F. Hiepe, and F. M. Pabst, Eds., pp. 147–149, 2nd edition, 2007. View at Google Scholar
  33. J. Savige, W. Dimech, M. Fritzler et al., “Addendum to the International consensus statement on testing and reporting of antineutrophil cytoplasmic antibodies: quality control guidelines, comments, and recommendations for testing in other autoimmune diseases,” American Journal of Clinical Pathology, vol. 120, no. 3, pp. 312–318, 2003. View at Publisher · View at Google Scholar · View at Scopus
  34. E. C. Hagen, M. R. Daha, J. Hermans et al., “Diagnostic value of standardized assays for anti-neutrophil cytoplasmic antibodies in idiopathic systemic vasculitis,” Kidney International, vol. 53, no. 3, pp. 743–753, 1998. View at Publisher · View at Google Scholar · View at Scopus
  35. J. Ludemann, E. Csernok, M. Ulmer et al., “Anti-neutrophil cytoplasm antibodies in Wegener's granulomatosis: immunodiagnostic value, monoclonal antibodies and characterization of the target antigen,” Netherlands Journal of Medicine, vol. 36, no. 3, pp. 157–162, 1990. View at Google Scholar · View at Scopus
  36. R. Goldschmeding, C. E. van der Schoot, D. Ten Bokkel Huinink et al., “Wegener's granulomatosis autoantibodies identify a novel diisopropylfluorophosphate-binding protein in the lysosomes of normal human neutrophils,” Journal of Clinical Investigation, vol. 84, no. 5, pp. 1577–1587, 1989. View at Google Scholar · View at Scopus
  37. A. Rutgers, J. Damoiseaux, C. Roozendaal, P. C. Limburg, C. A. Stegeman, and J. W. Cohen Tervaert, “ANCA-GBM dot-blot: evaluation of an assay in the differential diagnosis of patients presenting with rapidly progressive glomerulonephritis,” Journal of Clinical Immunology, vol. 24, no. 4, pp. 435–440, 2004. View at Publisher · View at Google Scholar · View at Scopus
  38. Ó. Arranz, J. Ara, R. Rodríguez et al., “Comparison of anti-PR3 capture and anti-PR3 direct ELISA for detection of antineutrophil cytoplasmic antibodies (ANCA) in long-term clinical follow-up of PR3-ANCA-associated vasculitis patients,” Clinical Nephrology, vol. 56, no. 4, pp. 295–301, 2001. View at Google Scholar · View at Scopus
  39. J. Sun, D. N. Fass, J. A. Hudson et al., “Capture-ELISA based on recombinant PR3 is sensitive for PR3-ANCA testing and allows detection of PR3 and PR3-ANCA/PR3 immunecomplexes,” Journal of Immunological Methods, vol. 211, no. 1-2, pp. 111–123, 1998. View at Publisher · View at Google Scholar · View at Scopus
  40. D. Roggenbuck, T. Buettner, L. Hoffmann, H. Schmechta, D. Reinhold, and K. Conrad, “High-sensitivity detection of autoantibodies against proteinase-3 by a novel third-generation enzyme-linked immunosorbent assay,” Annals of the New York Academy of Sciences, vol. 1173, pp. 41–46, 2009. View at Publisher · View at Google Scholar · View at Scopus
  41. J. U. Holle, E. Csernok, G. Fredenhagen, M. Backes, J. P. Bremer, and W. L. Gross, “Clinical evaluation of hsPR3-ANCA ELISA for detection of antineutrophil cytoplasmatic antibodies directed against proteinase 3,” Annals of the Rheumatic Diseases, vol. 69, no. 2, pp. 468–469, 2010. View at Publisher · View at Google Scholar · View at Scopus
  42. J. Damoiseaux, M. Vaessen, Y. Knapen et al., “Evaluation of the FIDIS vasculitis multiplex immunoassay for diagnosis and follow-up of ANCA-associated vasculitis and Goodpasture's disease,” Annals of the New York Academy of Sciences, vol. 1109, pp. 454–463, 2007. View at Publisher · View at Google Scholar · View at Scopus
  43. R. Kaul, K. Johnson, H. Scholz, and G. Marr, “Performance of the BioPlex 2200 Autoimmune Vasculitis kit,” Autoimmunity Reviews, vol. 8, no. 3, pp. 224–227, 2009. View at Publisher · View at Google Scholar · View at Scopus
  44. M. Trevisin, W. Pollock, W. Dimech, and J. Savige, “Evaluation of a multiplex flow cytometric immunoassay to detect PR3- and MPO-ANCA in active and treated vasculitis, and in inflammatory bowel disease (IBD),” Journal of Immunological Methods, vol. 336, no. 2, pp. 104–112, 2008. View at Publisher · View at Google Scholar · View at Scopus
  45. M. Mahler, A. Radice, W. Yang et al., “Development and performance evaluation of novel chemiluminescence assays for detection of anti-PR3 and anti-MPO antibodies,” Clinica Chimica Acta, vol. 413, no. 7-8, pp. 719–726, 2012. View at Publisher · View at Google Scholar · View at Scopus
  46. N. Bizzaro, A. Antico, S. Platzgummer et al., “Automated antinuclear immunofluorescence antibody screening: a comparative study of six computer-aided diagnostic systems,” Autoimmunity Reviews, vol. 13, pp. 292–298, 2014. View at Google Scholar
  47. C. Bonroy, C. Verfaillie, V. Smith et al., “Automated indirect immunofluorescence antinuclear antibody analysis is a standardized alternative for visual microscope interpretation,” Clinical Chemistry and Laboratory Medicine, vol. 51, pp. 1771–1779, 2013. View at Google Scholar
  48. S. Kivity, B. Gilburd, N. Agmon-Levin et al., “A novel automated indirect immunofluorescence autoantibody evaluation,” Clinical Rheumatology, vol. 31, no. 3, pp. 503–509, 2012. View at Publisher · View at Google Scholar · View at Scopus
  49. S. Schouwers, M. Bonnet, P. Verschueren et al., “Value-added reporting of antinuclear antibody testing by automated indirect immunofluorescence analysis,” Clinical Chemistry and Laboratory Medicine, vol. 52, pp. 547–551, 2014. View at Google Scholar
  50. J. Voigt, C. Krause, E. Rohwader et al., “Automated indirect immunofluorescence evaluation of antinuclear autoantibodies on HEp-2 cells,” Clinical and Developmental Immunology, vol. 2012, Article ID 651058, 7 pages, 2012. View at Publisher · View at Google Scholar
  51. G. Wang, E. Csernok, K. de Groot, and W. L. Gross, “Comparison of eight commercial kits for quantitation of antineutrophil cytoplasmic antibodies (ANCA),” Journal of Immunological Methods, vol. 208, no. 2, pp. 203–211, 1997. View at Publisher · View at Google Scholar · View at Scopus
  52. E. Csernok, D. Ahlquist, S. Ullrich, and W. L. Gross, “A critical evaluation of commercial immunoassays for antineutrophil cytoplasmic antibodies directed against proteinase 3 and myeloperoxidase in Wegener's granulomatosis and microscopic polyangiitis,” Rheumatology, vol. 41, no. 11, pp. 1313–1317, 2002. View at Google Scholar · View at Scopus
  53. E. Csernok, J. Holle, B. Hellmich et al., “Evaluation of capture ELISA for detection of antineutrophil cytoplasmic antibodies directed against proteinase 3 in Wegener's granulomatosis: first results from a multicentre study,” Rheumatology, vol. 43, no. 2, pp. 174–180, 2004. View at Publisher · View at Google Scholar · View at Scopus
  54. B. Hellmich, E. Csernok, G. Fredenhagen, and W. L. Gross, “A novel high sensitivity ELISA for detection of antineutrophil cytoplasm antibodies against proteinase-3,” Clinical and Experimental Rheumatology, vol. 25, no. 1, pp. S1–S5, 2007. View at Google Scholar · View at Scopus
  55. J. Damoiseaux, C. Dähnrich, A. Rosemann et al., “A novel enzyme-linked immunosorbent assay using a mixture of human native and recombinant proteinase-3 significantly improves the diagnostic potential for antineutrophil cytoplasmic antibody-associated vasculitis,” Annals of the Rheumatic Diseases, vol. 68, no. 2, pp. 228–233, 2009. View at Publisher · View at Google Scholar · View at Scopus
  56. N. Noel, C. Andre, D. Bengoufa et al., “Performance evaluation of three assays for the detection of PR3-ANCA in granulomatosis with polyangiitis in daily practice,” Autoimmunity Reviews, vol. 12, pp. 1118–1122, 2013. View at Google Scholar
  57. A. Radice, L. Bianchi, U. Maggiore, A. Vaglio, and R. A. Sinico, “Comparison of PR3-ANCA specific assay performance for the diagnosis of granulomatosis with polyangiitis (Wegener's),” Clinical Chemistry and Laboratory Medicine, vol. 51, pp. 2141–2149, 2013. View at Google Scholar
  58. G. A. Posthuma-Trumpie, J. Korf, and A. van Amerongen, “Lateral flow (immuno)assay: its strengths, weaknesses, opportunities and threats. A literature survey,” Analytical and Bioanalytical Chemistry, vol. 393, no. 2, pp. 569–582, 2009. View at Publisher · View at Google Scholar · View at Scopus
  59. J. Gordon and G. Michel, “Analytical sensitivity limits for lateral flow immunoassays,” Clinical Chemistry, vol. 54, no. 7, pp. 1250–1251, 2008. View at Publisher · View at Google Scholar · View at Scopus
  60. J. Bonenberger and M. Doumanas, “Overcoming sensitivity limitations of lateral-flow immunoassays with a novel labeling technique,” IVD Technology, 2006. View at Google Scholar
  61. J. Schulte-Pelkum, N. Offermann, and M. Fooke, “New highly sensitive and specific Lateral Flow Tests for the detection of Proteinase 3, Myeloperoxidase and Glomerular Basement Membrane antibodies,” in Proceedings of the 8th International Congress on Autoimmunity, p. 234, Granada, Spain, May 2012.
  62. R. Lucassen, J. Schulte-Pelkum, M. Petschinka, and M. Fooke, “New sensitive and reliable Lateral flow assay for the detection of proteinase 3 and myeloperoxidase antibodies,” in Proceedings of the 10th Dresden Symposium on Autoantibodies, pp. 694–695, 2011.
  63. M. Sowa, I. Knütter, R. Hiemann et al., “CytoBead ANCA—a novel indirect immunofluorescence test for the simultaneous detection of anti-neutrophil cytoplasmic antibodies,” in Proceedins of the 11th Dresden Symposium on Autoantibodies, pp. 271–272, Dresden, Germany, September 2013.
  64. M. Mahler, A. Radice, R. A. Sinico et al., “Performance evaluation of a novel chemiluminescence assay for detection of anti-GBM antibodies: an international multicenter study,” Nephrology Dialysis Transplantation, vol. 27, no. 1, pp. 243–252, 2012. View at Publisher · View at Google Scholar · View at Scopus
  65. M. Mahler, C. Bentow, A. Vizjak et al., “Multi-center evaluation of a novel chemiluminescent rapid assay for the detection of PR3-ANCA,” La Presse Médicale, vol. 42, pp. 683–684, 2013. View at Google Scholar
  66. T. Ito-Ihara, E. Muso, S. Kobayashi et al., “A comparative study of the diagnostic accuracy of ELISA systems for the detection of anti-neutrophil cytoplasm antibodies available in Japan and Europe,” Clinical and Experimental Rheumatology, vol. 26, no. 6, pp. 1027–1033, 2008. View at Google Scholar · View at Scopus
  67. B. Hellmich, O. Flossmann, W. L. Gross et al., “EULAR recommendations for conducting clinical studies and/or clinical trials in systemic vasculitis: focus on anti-neutrophil cytoplasm antibody-associated vasculitis,” Annals of the Rheumatic Diseases, vol. 66, no. 5, pp. 605–617, 2007. View at Publisher · View at Google Scholar · View at Scopus
  68. P. Vermeersch, S. Vervaeke, D. Blockmans et al., “Determination of anti-neutrophil cytoplasmic antibodies in small vessel vasculitis: comparative analysis of different strategies,” Clinica Chimica Acta, vol. 397, no. 1-2, pp. 77–81, 2008. View at Publisher · View at Google Scholar · View at Scopus
  69. S. M. Seck, B. Dussol, P. Brunet, and S. Burtey, “Clinical features and outcomes of ANCA-associated renal vasculitis,” Saudi Journal of Kidney Diseases and Transplantation, vol. 23, pp. 301–305, 2012. View at Google Scholar
  70. J. S. R. Sanders, P. M. Stassen, A. P. van Rossum, C. G. M. Kallenberg, and C. A. Stegeman, “Risk factors for relapse in anti-neutrophil cytoplasmic antibody (ANCA)-associated vasculitis: tools for treatment decisions?” Clinical and Experimental Rheumatology, vol. 22, no. 6, pp. S-94–S-101, 2004. View at Google Scholar · View at Scopus
  71. G. S. Hoffman, G. S. Kerr, R. Y. Leavitt et al., “Wegener granulomatosis: an analysis of 158 patients,” Annals of Internal Medicine, vol. 116, no. 6, pp. 488–498, 1992. View at Google Scholar · View at Scopus
  72. B. Terrier, D. Saadoun, D. Sène et al., “Antimyeloperoxidase antibodies are a useful marker of disease activity in antineutrophil cytoplasmic antibody-associated vasculitides,” Annals of the Rheumatic Diseases, vol. 68, no. 10, pp. 1564–1571, 2009. View at Publisher · View at Google Scholar · View at Scopus
  73. G. Luxton and R. Langham, “ANCA serology in the diagnosis and management of ANCA-associated renal vasculitis,” Nephrology, vol. 13, supplement 2, pp. S17–S23, 2008. View at Publisher · View at Google Scholar · View at Scopus
  74. D. Sinclair and J. M. Stevens, “Role of antineutrophil cytoplasmic antibodies and glomerular basement membrane antibodies in the diagnosis and monitoring of systemic vasculitides,” Annals of Clinical Biochemistry, vol. 44, no. 5, pp. 432–442, 2007. View at Publisher · View at Google Scholar · View at Scopus
  75. R. Birck, W. H. Schmitt, I. A. Kaelsch, and F. J. van der Woude, “Serial ANCA determinations for monitoring disease activity in patients with ANCA-associated vasculitis: systematic review,” American Journal of Kidney Diseases, vol. 47, no. 1, pp. 15–23, 2006. View at Publisher · View at Google Scholar · View at Scopus
  76. M. Papp, I. Altorjay, G. Lakos et al., “Evaluation of the combined application of ethanol-fixed and formaldehyde-fixed neutrophil substrates for identifying atypical perinuclear antineutrophil cytoplasmic antibodies in inflammatory bowel disease,” Clinical and Vaccine Immunology, vol. 16, no. 4, pp. 464–470, 2009. View at Publisher · View at Google Scholar · View at Scopus
  77. M. Papp, G. L. Norman, I. Altorjay, and P. L. Lakatos, “Utility of serological markers in inflammatory bowel diseases: gadget or magic?” World Journal of Gastroenterology, vol. 13, no. 14, pp. 2028–2036, 2007. View at Google Scholar · View at Scopus
  78. G. E. Reese, V. A. Constantinides, C. Simillis et al., “Diagnostic precision of anti-Saccharomyces cerevisiae antibodies and perinuclear antineutrophil cytoplasmic antibodies in inflammatory bowel disease,” American Journal of Gastroenterology, vol. 101, no. 10, pp. 2410–2422, 2006. View at Publisher · View at Google Scholar · View at Scopus
  79. X. Bossuyt, “Serologic markers in inflammatory bowel disease,” Clinical Chemistry, vol. 52, no. 2, pp. 171–181, 2006. View at Publisher · View at Google Scholar · View at Scopus
  80. J.-F. Quinton, B. Sendid, D. Reumaux et al., “Anti-Saccharomyces cerevisiae manna antibodies combined with antineutrophil cytoplasmic autoantibodies in inflammatory bowel disease: prevalence and diagnostic role,” Gut, vol. 42, no. 6, pp. 788–791, 1998. View at Google Scholar · View at Scopus
  81. M. Ferrante, L. Henckaerts, M. Joossens et al., “New serological markers in inflammatory bowel disease are associated with complicated disease behaviour,” Gut, vol. 56, no. 10, pp. 1394–1403, 2007. View at Publisher · View at Google Scholar · View at Scopus
  82. E. Israeli, I. Grotto, B. Gilburd et al., “Anti-Saccharomyces cerevisiae and antineutrophil cytoplasmic antibodies as predictors of inflammatory bowel disease,” Gut, vol. 54, no. 9, pp. 1232–1236, 2005. View at Publisher · View at Google Scholar · View at Scopus
  83. B. Terjung, U. Spengler, T. Sauerbruch, and H. J. Worman, “'Atypical p-ANCA' in IBD and hepatobiliary disorders react with a 50-kilodalton nuclear envelope protein of neutrophils and myeloid cell lines,” Gastroenterology, vol. 119, no. 2, pp. 310–322, 2000. View at Google Scholar · View at Scopus
  84. C. Mowat, A. Cole, A. Windsor et al., “Guidelines for the management of inflammatory bowel disease in adults,” Gut, vol. 60, no. 5, pp. 571–607, 2011. View at Publisher · View at Google Scholar · View at Scopus
  85. D. Roggenbuck, G. Hausdorf, L. Martinez-Gamboa et al., “Identification of GP2, the major zymogen granule membrane glycoprotein, as the autoantigen of pancreatic antibodies in Crohn's disease,” Gut, vol. 58, no. 12, pp. 1620–1628, 2009. View at Publisher · View at Google Scholar · View at Scopus
  86. D. P. Bogdanos, E. I. Rigopoulou, D. S. Smyk et al., “Diagnostic value, clinical utility and pathogenic significance of reactivity to the molecular targets of Crohn's disease specific-pancreatic autoantibodies,” Autoimmunity Reviews, vol. 11, pp. 143–148, 2011. View at Publisher · View at Google Scholar · View at Scopus
  87. K. O. de Beéck, S. Vermeire, P. Rutgeerts, and X. Bossuyt, “Antibodies to GP2, the major zymogen granule membrane glycoprotein, in inflammatory bowel diseases,” Gut, vol. 61, no. 1, pp. 162–164, 2012. View at Publisher · View at Google Scholar · View at Scopus
  88. K. Op de Beéck, K. van den Bergh, S. Vermeire et al., “Immune reactivity to β-tubulin isotype 5 and vesicular integralmembrane protein 36 in patients with autoimmune gastrointestinal disorders,” Gut, vol. 60, no. 11, pp. 1601–1602, 2011. View at Publisher · View at Google Scholar · View at Scopus
  89. M. Vecchi, M. B. Bianchi, R. A. Sinico et al., “Antibodies to neutrophil cytoplasm in Italian patients with ulcerative colitis: sensitivity, specificity and recognition of putative antigens,” Digestion, vol. 55, no. 1, pp. 34–39, 1994. View at Google Scholar · View at Scopus
  90. C. J. Ooi, B. L. Lim, W. K. Cheong, A. E. Ling, and H. S. Ng, “Antineutrophil cytoplasmic antibodies (ANCAs) in patients with inflammatory bowel disease show no correlation with proteinase 3, lactoferrin, myeloperoxidase, elastase, cathepsin G and lysozyme: a Singapore study,” Annals of the Academy of Medicine Singapore, vol. 29, no. 6, pp. 704–707, 2000. View at Google Scholar · View at Scopus
  91. A. N. Elzouki, S. Eriksson, R. Lofberg, L. Nassberger, J. Wieslander, and S. Lindgren, “The prevalence and clinical significance of α1-antitrypsin deficiency (PiZ) and ANCA specificities (proteinase 3, BPI) in patients with ulcerative colitis,” Inflammatory Bowel Diseases, vol. 5, no. 4, pp. 246–252, 1999. View at Google Scholar · View at Scopus
  92. J. Xu, C.-H. Yang, X.-Y. Chen, X.-H. Li, M. Dai, and S.-D. Xiao, “A subset of ulcerative colitis with positive proteinase-3 antineutrophil cytoplasmic antibody,” World Journal of Gastroenterology, vol. 14, no. 45, pp. 7012–7015, 2008. View at Publisher · View at Google Scholar · View at Scopus
  93. K. Tsiveriotis, A. Tsirogianni, E. Pipi, K. Soufleros, and C. Papasteriades, “Antineutrophil cytoplasmic antibodies testing in a large cohort of unselected greek patients,” Autoimmune Disorders, vol. 2011, Article ID 626495, 9 pages, 2011. View at Publisher · View at Google Scholar
  94. S. Joossens, W. Reinisch, S. Vermeire et al., “The value of serologic markers in indeterminate colitis: a prospective follow-up study,” Gastroenterology, vol. 122, no. 5, pp. 1242–1247, 2002. View at Google Scholar · View at Scopus
  95. K. Geboes, J.-F. Colombel, A. Greenstein et al., “Indeterminate colitis: a review of the concept—what's in a name?” Inflammatory Bowel Diseases, vol. 14, no. 6, pp. 850–857, 2008. View at Publisher · View at Google Scholar · View at Scopus
  96. J. M. Civan, C. R. Gilbert, and D. M. Kastenberg, “Pulmonary capillaritis: a rare extra-intestinal manifestation of inflammatory bowel disease,” American Journal of Gastroenterology, vol. 106, no. 4, pp. 804–805, 2011. View at Publisher · View at Google Scholar · View at Scopus
  97. E. Beccastrini, G. Emmi, D. Squatrito, G. Nesi, F. Almerigogna, and L. Emmi, “Lobular panniculitis with small vessel vasculitis associated with ulcerative colitis,” Modern Rheumatology, vol. 21, no. 5, pp. 528–531, 2011. View at Publisher · View at Google Scholar · View at Scopus
  98. Q. Qian, L. Cornell, V. Chandan, R. Hartman, and S. Caples, “Hemorrhagic colitis as a presenting feature of Wegener granulomatosis,” Journal of Gastrointestinal and Liver Diseases, vol. 19, no. 4, pp. 445–447, 2010. View at Google Scholar · View at Scopus
  99. M. J. Amador-Patarroyo, J. G. Arbelaez, R. D. Mantilla et al., “Sjogren's syndrome at the crossroad of polyautoimmunity,” Journal of Autoimmunity, vol. 39, pp. 199–205, 2012. View at Google Scholar
  100. C. Pagnoux, A. Mahr, P. Cohen, and L. Guillevin, “Presentation and outcome of gastrointestinal involvement in systemic necrotizing vasculitides: analysis of 62 patients with polyarteritis nodosa, microscopic polyangiitis, Wegener granulomatosis, Churg-Strauss syndrome, or rheumatoid arthritis-associated vasculitis,” Medicine, vol. 84, no. 2, pp. 115–128, 2005. View at Publisher · View at Google Scholar · View at Scopus
  101. A. P. Burke, L. H. Sobin, and R. Virmani, “Localized vasculitis of the gastrointestinal tract,” American Journal of Surgical Pathology, vol. 19, no. 3, pp. 338–349, 1995. View at Google Scholar · View at Scopus