Relapse Predictors in Antineutrophil Cytoplasmic Antibody (ANCA)-Associated Vasculitis
Abstract
:1. Introduction
2. Methodology
3. Baseline Relapse Risk Evaluation
3.1. ANCA Testing
3.2. Cell Count, Genetics, Infections, Histopathology and Other Predictors at Baseline
4. Relapse Predictors on Remission
4.1. ANCA Testing
4.2. B-Cell Reconstitution
4.3. Other Potential Markers
5. Discussion
6. Conclusions
Author Contributions
Funding
Conflicts of Interest
References
- Gonzalez-Gay, M.A.; Garcia-Porrua, C.; Guerrero, J.; Rodriguez-Ledo, P.; Llorca, J. The Epidemiology of the Primary Systemic Vasculitides in Northwest Spain: Implications of the Chapel Hill Consensus Conference Definitions. Arthritis Rheum. 2003, 49, 388–393. [Google Scholar] [CrossRef] [PubMed]
- Watts, R.A.; Lane, S.E.; Bentham, G.; Scott, D.G. Epidemiology of Systemic Vasculitis: A Ten-Year Study in the United Kingdom. Arthritis Rheum. 2000, 43, 414–419. [Google Scholar] [CrossRef]
- Mohammad, A.J.; Jacobsson, L.T.; Westman, K.W.; Sturfelt, G.; Segelmark, M. Incidence and Survival Rates in Wegener’s Granulomatosis, Microscopic Polyangiitis, Churg-Strauss Syndrome, and Polyarteritis Nodosa. Rheumatology 2009, 48, 1560–1565. [Google Scholar] [CrossRef] [PubMed]
- Jennette, J.C.; Falk, R.J.; Bacon, P.A.; Basu, N.; Cid, M.C.; Ferrario, F.; Flores-Suarez, L.F.; Gross, W.L.; Guillevin, L.; Hagen, E.C.; et al. 2012 Revised International Chapel Hill Consensus Conference Nomenclature of Vasculitides. Arthritis Rheum. 2013, 65, 1–11. [Google Scholar] [CrossRef]
- Mohammad, A.J. An Update on the Epidemiology of ANCA-Associated Vasculitis. Rheumatology 2020, 59 (Suppl. S3), 42–50. [Google Scholar] [CrossRef]
- Walton, E.W. Giant-Cell Granuloma of the Respiratory Tract (Wegener’s Granulomatosis). Br. Med. J. 1958, 2, 265–270. [Google Scholar] [CrossRef]
- Tan, J.A.; Dehghan, N.; Chen, W.; Xie, H.; Esdaile, J.M.; Avina-Zubieta, J.A. Mortality in ANCA-Associated Vasculitis: A Meta-Analysis of Observational Studies. Ann. Rheum. Dis. 2017, 76, 1566–1574. [Google Scholar] [CrossRef]
- Hellmich, B.; Sanchez-Alamo, B.; Schirmer, J.H.; Berti, A.; Blockmans, D.; Cid, M.C.; Holle, J.U.; Hollinger, N.; Karadag, O.; Kronbichler, A.; et al. EULAR Recommendations for the Management of ANCA-Associated Vasculitis: 2022 Update. Ann. Rheum. Dis. 2024, 83, 30–47. [Google Scholar] [CrossRef] [PubMed]
- Robson, J.; Doll, H.; Suppiah, R.; Flossmann, O.; Harper, L.; Höglund, P.; Jayne, D.; Mahr, A.; Westman, K.; Luqmani, 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. [Google Scholar] [CrossRef]
- Terrier, B.; Darbon, R.; Durel, C.A.; Hachulla, E.; Karras, A.; Maillard, H.; Papo, T.; Puechal, X.; Pugnet, G.; Quemeneur, T.; et al. French Recommendations for the Management of Systemic Necrotizing Vasculitides (Polyarteritis Nodosa and ANCA-Associated Vasculitides). Orphanet J. Rare Dis. 2020, 15, 351. [Google Scholar] [CrossRef]
- Yates, M.; Watts, R.A.; Bajema, I.M.; Cid, M.C.; Crestani, B.; Hauser, T.; Hellmich, B.; Holle, J.U.; Laudien, M.; Little, M.A.; et al. EULAR/ERA-EDTA Recommendations for the Management of ANCA-Associated Vasculitis. Ann. Rheum. Dis. 2016, 75, 1583–1594. [Google Scholar] [CrossRef] [PubMed]
- Cao, Y.; Tian, Z.; Li, W.; Ma, L.; Yu, Y.; Ren, W. Predictors of Treatment Resistance and Relapse in Chinese Patients with Antineutrophil Cytoplasmic Antibody-Associated Disease. J. Rheumatol. 2014, 41, 916–922. [Google Scholar] [CrossRef]
- Hassan, T.M.; Hassan, A.S.; Igoe, A.; Logan, M.; Gunaratnam, C.; McElvaney, N.G.; O’Neill, S.J. Lung Involvement at Presentation Predicts Disease Activity and Permanent Organ Damage at 6, 12 and 24 Months Follow-Up in ANCA-Associated Vasculitis. BMC Immunol. 2014, 15, 20. [Google Scholar] [CrossRef] [PubMed]
- Pagnoux, C.; Hogan, S.L.; Chin, H.; Jennette, J.C.; Falk, R.J.; Guillevin, L.; Nachman, P.H. Predictors of Treatment Resistance and Relapse in Antineutrophil Cytoplasmic Antibody-Associated Small-Vessel Vasculitis: Comparison of Two Independent Cohorts. Arthritis Rheum. 2008, 58, 2908–2918. [Google Scholar] [CrossRef] [PubMed]
- Walsh, M.; Flossmann, O.; Berden, A.; Westman, K.; Höglund, P.; Stegeman, C.; Jayne, D.; European Vasculitis Study Group. Risk Factors for Relapse of Antineutrophil Cytoplasmic Antibody-Associated Vasculitis. Arthritis Rheum. 2012, 64, 542–548. [Google Scholar] [CrossRef] [PubMed]
- King, C.; Druce, K.L.; Nightingale, P.; Kay, E.; Basu, N.; Salama, A.D.; Harper, L. Predicting Relapse in Anti-Neutrophil Cytoplasmic Antibody-Associated Vasculitis: A Systematic Review and Meta-Analysis. Rheumatol. Adv. Pract. 2021, 5, rkab018. [Google Scholar] [CrossRef]
- He, P.; Hu, J.P.; Tian, X.J.; He, L.J.; Sun, S.R.; Huang, C. Prevalence and risk factors of relapse in patients with ANCA-associated vasculitis receiving cyclophosphamide induction: A systematic review and meta-analysis of large observational studies. Rheumatology 2021, 60, 1067–1079. [Google Scholar] [CrossRef] [PubMed]
- Wójcik, K.; Ćmiel, B.; Kułakowski, P.; Janowski, L.; Wawrzycka-Adamczyk, K.; Korkosz, M.; Masiak, A.; Zdrojewski, Z.; Bułło-Piontecka, B.; Dębska-Ślizień, A.; et al. Identification of ANCA-Associated Vasculitis Relapse Risk Factors for Building a Personalized Maintenance Therapy Scheme Model. Ann. Rheum. Dis. 2024, 83, 184. [Google Scholar]
- Jennette, J.C.; Falk, R.J. Pathogenesis of Antineutrophil Cytoplasmic Autoantibody-Mediated Disease. Nat. Rev. Rheumatol. 2014, 10, 463–473. [Google Scholar] [CrossRef]
- Bossuyt, X.; Rasmussen, N.; van Paassen, P.; Hellmich, B.; Baslund, B.; Vermeersch, P.; Blockmans, D.; Cohen Tervaert, J.W.; Csernok, E.; Damoiseaux, J. A Multicentre Study to Improve Clinical Interpretation of Proteinase-3 and Myeloperoxidase Anti-Neutrophil Cytoplasmic Antibodies. Rheumatology 2017, 56, 1533–1541. [Google Scholar] [CrossRef]
- Damoiseaux, J.; Csernok, E.; Rasmussen, N.; Moosig, F.; van Paassen, P.; Baslund, B.; Vermeersch, P.; Blockmans, D.; Cohen Tervaert, J.W.; Bossuyt, X. Detection of Antineutrophil Cytoplasmic Antibodies (ANCAs): A Multicentre European Vasculitis Study Group (EUVAS) Evaluation of the Value of Indirect Immunofluorescence (IIF) versus Antigen-Specific Immunoassays. Ann. Rheum. Dis. 2017, 76, 647–653. [Google Scholar] [CrossRef] [PubMed]
- Bossuyt, X.; Cohen Tervaert, J.W.; Arimura, Y.; Blockmans, D.; Flores-Suárez, L.F.; Guillevin, L.; Hellmich, B.; Jayne, D.; Jennette, J.C.; Kallenberg, C.G.M.; et al. Position Paper: Revised 2017 International Consensus on Testing of ANCAs in Granulomatosis with Polyangiitis and Microscopic Polyangiitis. Nat. Rev. Rheumatol. 2017, 13, 683–692. [Google Scholar] [CrossRef] [PubMed]
- Suppiah, R.; Robson, J.C.; Grayson, P.C.; Ponte, C.; Craven, A.; Khalid, S.; Judge, A.; Hutchings, A.; Merkel, P.A.; Luqmani, R.A.; et al. American College of Rheumatology/European Alliance of Associations for Rheumatology Classification Criteria for Microscopic Polyangiitis. Arthritis Rheumatol. 2022, 74, 400–406. [Google Scholar] [CrossRef] [PubMed]
- Robson, J.C.; Grayson, P.C.; Ponte, C.; Suppiah, R.; Craven, A.; Judge, A.; Khalid, S.; Hutchings, A.; Watts, R.A.; Merkel, P.A.; et al. 2022 American College of Rheumatology/European Alliance of Associations for Rheumatology classification criteria for granulomatosis with polyangiitis. Ann. Rheum. Dis. 2022, 81, 315–320. [Google Scholar] [CrossRef]
- Grayson, P.C.; Ponte, C.; Suppiah, R.; Robson, J.C.; Craven, A.; Judge, A.; Khalid, S.; Hutchings, A.; Luqmani, R.A.; Watts, R.A.; et al. 2022 American College of Rheumatology/European Alliance of Associations for Rheumatology Classification Criteria for Eosinophilic Granulomatosis with Polyangiitis. Ann. Rheum. Dis. 2022, 81, 309–314. [Google Scholar] [CrossRef]
- Holle, J.U.; Gross, W.L.; Holl-Ulrich, K.; Ambrosch, P.; Noelle, B.; Both, M.; Csernok, E.; Moosig, F.; Schinke, S.; Reinhold-Keller, E. Prospective long-term follow-up of patients with localised Wegener’s granulomatosis: Does it occur as persistent disease stage? Ann. Rheum. Dis. 2010, 69, 1934–1939. [Google Scholar] [CrossRef]
- Bossuyt, X. Serologic markers in inflammatory bowel disease. Clin. Chem. 2006, 52, 171–181. [Google Scholar] [CrossRef]
- Pendergraft, W.F.; Niles, J.L. Trojan horses: Drug culprits associated with antineutrophil cytoplasmic autoantibody (ANCA) vasculitis. Curr. Opin. Rheumatol. 2014, 26, 42–49. [Google Scholar] [CrossRef]
- Kitching, A.R.; Anders, H.J.; Basu, N.; Brouwer, E.; Gordon, J.; Jayne, D.R.; Kullman, J.; Lyons, P.A.; Merkel, P.A.; Savage, C.O.S.; et al. ANCA-associated vasculitis. Nat. Rev. Dis. Primers 2020, 6, 71. [Google Scholar] [CrossRef]
- Chang, D.-Y.; Li, Z.-Y.; Chen, M.; Zhao, M.H. Myeloperoxidase-ANCA-positive granulomatosis with polyangiitis is a distinct subset of ANCA-associated vasculitis: A retrospective analysis of 455 patients from a single center in China. Semin. Arthritis Rheum. 2019, 48, 701–706. [Google Scholar] [CrossRef]
- Moiseev, S.; Cohen Tervaert, J.W.; Arimura, Y.; Bogdanos, D.P.; Csernok, E.; Damoiseaux, J.; Ferrante, M.; Flores-Suárez, L.F.; Fritzler, M.J.; Invernizzi, P.; et al. 2020 international consensus on ANCA testing beyond systemic vasculitis. Autoimmun. Rev. 2020, 19, 102618. [Google Scholar] [CrossRef]
- Kyndt, X.; Reumaux, D.; Bridoux, F.; Tribout, B.; Bataille, P.; Hachulla, E.; Hatron, P.Y.; Duthilleul, P.; Vanhille, P. Serial measurements of antineutrophil cytoplasmic autoantibodies in patients with systemic vasculitis. Am. J. Med. 1999, 106, 527–533. [Google Scholar] [CrossRef] [PubMed]
- Hogan, S.L.; Falk, R.J.; Chin, H.; Cai, J.; Jennette, C.E.; Jennette, J.C.; Nachman, P.H. Predictors of relapse and treatment resistance in antineutrophil cytoplasmic antibody-associated small-vessel vasculitis. Ann. Intern. Med. 2005, 143, 621–631. [Google Scholar] [CrossRef] [PubMed]
- Schirmer, J.H.; Wright, M.N.; Herrmann, K.; Laudien, M.; Nölle, B.; Reinhold-Keller, E.; Bremer, J.P.; Moosig, F.; Holle, J.U. Myeloperoxidase-Antineutrophil Cytoplasmic Antibody (ANCA)-Positive Granulomatosis With Polyangiitis (Wegener’s) Is a Clinically Distinct Subset of ANCA-Associated Vasculitis: A Retrospective Analysis of 315 Patients From a German Vasculitis Referral Center. Arthritis Rheumatol. 2016, 68, 2953–2963. [Google Scholar]
- Puéchal, X.; Pagnoux, C.; Perrodeau, É.; Hamidou, M.; Boffa, J.J.; Kyndt, X.; Lifermann, F.; Papo, T.; Merrien, D.; Smail, A.; et al. Long-Term Outcomes Among Participants in the WEGENT Trial of Remission-Maintenance Therapy for Granulomatosis With Polyangiitis (Wegener’s) or Microscopic Polyangiitis. Arthritis Rheumatol. 2016, 68, 690–701. [Google Scholar] [CrossRef] [PubMed]
- Iudici, M.; Pagnoux, C.; Courvoisier, D.S.; Cohen, P.; Hamidou, M.; Aouba, A.; Lifermann, F.; Ruivard, M.; Aumaître, O.; Bonnotte, B.; et al. Granulomatosis with polyangiitis: Study of 795 patients from the French Vasculitis Study Group registry. Semin. Arthritis Rheum. 2021, 51, 339–346. [Google Scholar] [CrossRef]
- Lionaki, S.; Blyth, E.R.; Hogan, S.L.; Hu, Y.; Senior, B.A.; Jennette, C.E.; Nachman, P.H.; Jennette, J.C.; Falk, R.J. 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. 2012, 64, 3452–3462. [Google Scholar] [CrossRef]
- Mahr, A.; Katsahian, S.; Varet, H.; Guillevin, L.; Hagen, E.C.; Höglund, P.; Merkel, P.A.; Pagnoux, C.; Rasmussen, N.; Westman, K.; et al. Revisiting the classification of clinical phenotypes of anti-neutrophil cytoplasmic antibody-associated vasculitis: A cluster analysis. Ann. Rheum. Dis. 2013, 72, 1003–1010. [Google Scholar] [CrossRef]
- Miloslavsky, E.M.; Specks, U.; Merkel, P.A.; Seo, P.; Spiera, R.; Langford, C.A.; Hoffman, G.S.; Kallenberg, C.G.; St Clair, E.W.; Tchao, N.K.; et al. Clinical outcomes of remission induction therapy for severe antineutrophil cytoplasmic antibody-associated vasculitis. Arthritis Rheum. 2013, 65, 2441–2449. [Google Scholar] [CrossRef]
- Ono, N.; Niiro, H.; Ueda, A.; Sawabe, T.; Nishizaka, H.; Furugo, I.; Yoshizawa, S.; Yoshizawa, S.; Tsukamoto, H.; Kiyohara, C.; et al. Characteristics of MPO-ANCA-positive granulomatosis with polyangiitis: A retrospective multi-center study in Japan. Rheumatol. Int. 2015, 35, 555–559. [Google Scholar] [CrossRef]
- Miloslavsky, E.M.; Lu, N.; Unizony, S.; Choi, H.K.; Merkel, P.A.; Seo, P.; Spiera, R.; Langford, C.A.; Hoffman, G.S.; Kallenberg, C.G.; et al. Myeloperoxidase-Antineutrophil Cytoplasmic Antibody (ANCA)-Positive and ANCA-Negative Patients With Granulomatosis With Polyangiitis (Wegener’s): Distinct Patient Subsets. Arthritis Rheumatol. 2016, 68, 2945–2952. [Google Scholar] [CrossRef] [PubMed]
- Deshayes, S.; Martin Silva, N.; Khoy, K.; Yameogo, S.; Mariotte, D.; Lobbedez, T.; Aouba, A. Clinical impact of subgrouping ANCA-associated vasculitis according to antibody specificity beyond the clinicopathological classification. Rheumatology 2019, 58, 1731–1739. [Google Scholar] [CrossRef]
- Puéchal, X.; Iudici, M.; Pagnoux, C.; Cohen, P.; Hamidou, M.; Aouba, A.; Lifermann, F.; Ruivard, M.; Aumaître, O.; Bonnotte, B.; et al. Comparative study of granulomatosis with polyangiitis subsets according to ANCA status: Data from the French Vasculitis Study Group Registry. RMD Open. 2022, 8, e002160. [Google Scholar] [CrossRef] [PubMed]
- von Borstel, A.; Land, J.; Abdulahad, W.H.; Rutgers, A.; Stegeman, C.A.; Diepstra, A.; Heeringa, P.; Sanders, J.S. CD27+CD38hi B Cell Frequency During Remission Predicts Relapsing Disease in Granulomatosis With Polyangiitis Patients. Front. Immunol. 2019, 10, 2221. [Google Scholar] [CrossRef] [PubMed]
- Grayson, P.C.; Carmona-Rivera, C.; Xu, L.; Lim, N.; Gao, Z.; Asare, A.L.; Specks, U.; Stone, J.H.; Seo, P.; Spiera, R.F.; et al. Neutrophil-Related Gene Expression and Low-Density Granulocytes Associated With Disease Activity and Response to Treatment in Antineutrophil Cytoplasmic Antibody-Associated Vasculitis. Arthritis Rheumatol. 2015, 67, 1922–1932. [Google Scholar] [CrossRef]
- Li, W.; Huang, H.; Cai, M.; Yuan, T.; Sheng, Y. Antineutrophil Cytoplasmic Antibody-Associated Vasculitis Update: Genetic Pathogenesis. Front. Immunol. 2021, 12, 624848. [Google Scholar] [CrossRef]
- Alberici, F.; Smith, R.M.; Fonseca, M.; Willcocks, L.C.; Jones, R.B.; Holle, J.U.; Wieczorek, S.; Neumann, T.; Martorana, D.; Gregorini, G.; 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, 1684–1687. [Google Scholar] [CrossRef]
- Chang, D.Y.; Luo, H.; Zhou, X.J.; Chen, M.; Zhao, M.H. Association of HLA Genes with Clinical Outcomes of ANCA-Associated Vasculitis. Clin. J. Am. Soc. Nephrol. 2012, 7, 1293–1299. [Google Scholar] [CrossRef]
- Hilhorst, M.; Arndt, F.; Joseph Kemna, M.; Wieczorek, S.; Donner, Y.; Wilde, B.; Thomas Epplen, J.; van Paassen, P.; Cohen Tervaert, J.W. HLA-DPB1 as a Risk Factor for Relapse in Antineutrophil Cytoplasmic Antibody-Associated Vasculitis: A Cohort Study. Arthritis Rheumatol. 2016, 68, 1721–1730. [Google Scholar] [CrossRef]
- Stegeman, C.A.; Tervaert, J.W.; Sluiter, W.J.; Manson, W.L.; de Jong, P.E.; Kallenberg, C.G. Association of Chronic Nasal Carriage of Staphylococcus aureus and Higher Relapse Rates in Wegener Granulomatosis. Ann. Intern. Med. 1994, 120, 12–17. [Google Scholar] [CrossRef]
- Popa, E.R.; Stegeman, C.A.; Abdulahad, W.H.; van der Meer, B.; Arends, J.; Manson, W.M.; Bos, N.A.; Kallenberg, C.G.; Tervaert, J.W. Staphylococcal Toxic-Shock-Syndrome-Toxin-1 as a Risk Factor for Disease Relapse in Wegener’s Granulomatosis. Rheumatology 2007, 46, 1029–1033. [Google Scholar] [CrossRef]
- Stegeman, C.A.; Cohen Tervaert, J.W.; de Jong, P.E.; Kallenberg, C.G. Trimethoprim–Sulfamethoxazole for the Prevention of Relapses of Wegener’s Granulomatosis. N. Engl. J. Med. 1996, 335, 16–20. [Google Scholar] [CrossRef] [PubMed]
- Laudien, M.; Häsler, R.; Wohlers, J.; Böck, J.; Lipinski, S.; Bremer, L.; Podschun, R.; Ambrosch, P.; Lamprecht, P.; Rosenstiel, P.; et al. Molecular signatures of a disturbed nasal barrier function in the primary tissue of Wegener’s granulomatosis. Mucosal Immunol. 2011, 4, 564–573. [Google Scholar] [CrossRef]
- Grayson, P.C.; Steiling, K.; Platt, M.; Berman, J.S.; Zhang, X.; Xiao, J.; Alekseyev, Y.O.; Liu, G.; Monach, P.A.; Kaplan, M.J.; et al. Defining the Nasal Transcriptome in Granulomatosis with Polyangiitis (Wegener’s). Arthritis Rheumatol. 2015, 67, 2233–2239. [Google Scholar] [CrossRef]
- Ooi, J.D.; Jiang, J.H.; Eggenhuizen, P.J.; Chua, L.L.; Van Timmeren, M.; Loh, K.L.; O’Sullivan, K.M.; Gan, P.Y.; Zhong, Y.; Tsyganov, K.; et al. A Plasmid-Encoded Peptide from Staphylococcus aureus Induces Anti-Myeloperoxidase Nephritogenic Autoimmunity. Nat. Commun. 2019, 10, 3392. [Google Scholar] [CrossRef]
- Berden, A.E.; Ferrario, F.; Hagen, E.C.; Jayne, D.R.; Jennette, J.C.; Joh, K.; Neumann, I.; Noël, L.H.; Pusey, C.D.; Waldherr, R.; et al. Histopathologic classification of ANCA-associated glomerulonephritis. J. Am. Soc. Nephrol. 2010, 21, 1628–1636. [Google Scholar] [CrossRef] [PubMed]
- Chang, D.Y.; Wu, L.H.; Liu, G.; Chen, M.; Kallenberg, C.G.M.; Zhao, M.H. Re-evaluation of the Histopathologic Classification of ANCA-Associated Glomerulonephritis: A Study of 121 Patients in a Single Center. Nephrol. Dial. Transplant. 2012, 27, 2343–2349. [Google Scholar] [CrossRef] [PubMed]
- Muso, E.; Endo, T.; Itabashi, M.; Kakita, H.; Iwasaki, Y.; Tateishi, Y.; Komiya, T.; Ihara, T.; Yumura, W.; Sugiyama, T.; et al. Evaluation of the newly proposed simplified histological classification in Japanese cohorts of myeloperoxidase-anti-neutrophil cytoplasmic antibody-associated glomerulonephritis in comparison with other Asian and European cohorts. Clin. Exp. Nephrol. 2013, 17, 659–662. [Google Scholar] [CrossRef]
- Göçeroğlu, A.; Berden, A.E.; Fiocco, M.; Floßmann, O.; Westman, K.W.; Ferrario, F.; Gaskin, G.; Pusey, C.D.; Hagen, E.C.; Noël, L.-H.; et al. ANCA-Associated Glomerulonephritis: Risk Factors for Renal Relapse. PLoS ONE 2016, 11, e0165402. [Google Scholar] [CrossRef]
- Brix, S.R.; Stege, G.; Disteldorf, E.; Hoxha, E.; Krebs, C.; Krohn, S.; Otto, B.; Klätschke, K.; Herden, E.; Heymann, F.; et al. CC Chemokine Ligand 18 in ANCA-Associated Crescentic GN. J. Am. Soc. Nephrol. 2015, 26, 2105–2117. [Google Scholar] [CrossRef]
- Pepper, R.J.; Draibe, J.B.; Caplin, B.; Fervenza, F.C.; Hoffman, G.S.; Kallenberg, C.G.; Langford, C.A.; Monach, P.A.; Seo, P.; Spiera, R.; et al. Association of Serum Calprotectin (S100A8/A9) Level with Disease Relapse in Proteinase 3-Antineutrophil Cytoplasmic Antibody-Associated Vasculitis. Arthritis Rheumatol. 2017, 69, 185–193. [Google Scholar] [CrossRef] [PubMed]
- Závada, J.; Kideryová, L.; Pytlík, R.; Hrusková, Z.; Tesar, V. Reduced Number of Endothelial Progenitor Cells is Predictive of Early Relapse in Anti-Neutrophil Cytoplasmic Antibody-Associated Vasculitis. Rheumatology 2009, 48, 1197–1201. [Google Scholar] [CrossRef] [PubMed]
- Monach, P.A.; Warner, R.L.; Lew, R.; Tómasson, G.; Specks, U.; Stone, J.H.; Fervenza, F.C.; Hoffman, G.S.; Kallenberg, C.G.M.; Langford, C.A. Serum Biomarkers of Disease Activity in Longitudinal Assessment of Patients with ANCA-Associated Vasculitis. ACR Open Rheumatol. 2022, 4, 168–176. [Google Scholar] [CrossRef] [PubMed]
- Grayson, P.C.; Monach, P.A.; Pagnoux, C.; Cuthbertson, D.; Carette, S.; Hoffman, G.S.; Khalidi, N.A.; Koening, C.L.; Langford, C.A.; Maksimowicz-McKinnon, K.; et al. Value of Commonly Measured Laboratory Tests as Biomarkers of Disease Activity and Predictors of Relapse in Eosinophilic Granulomatosis with Polyangiitis. Rheumatology 2015, 54, 1351–1359. [Google Scholar] [CrossRef]
- Yang, J.J.; Preston, G.A.; Pendergraft, W.F.; Segelmark, M.; Heeringa, P.; Hogan, S.L.; Jennette, J.C.; Falk, R.J. Internalization of Proteinase 3 is Concomitant with Endothelial Cell Apoptosis and Internalization of Myeloperoxidase with Generation of Intracellular Oxidants. Am. J. Pathol. 2001, 158, 581–592. [Google Scholar] [CrossRef]
- Xiao, H.; Heeringa, P.; Hu, P.; Liu, Z.; Zhao, M.; Aratani, Y.; Maeda, N.; Falk, R.J.; Jennette, J.C. Antineutrophil Cytoplasmic Autoantibodies Specific for Myeloperoxidase Cause Glomerulonephritis and Vasculitis in Mice. J. Clin. Investig. 2002, 110, 955–963. [Google Scholar] [CrossRef]
- Little, M.A.; Smyth, C.L.; Yadav, R.; Ambrose, L.; Cook, H.T.; Nourshargh, S.; Pusey, C.D. Antineutrophil Cytoplasm Antibodies Directed Against Myeloperoxidase Augment Leukocyte-Microvascular Interactions In Vivo. Blood 2005, 106, 2050–2058. [Google Scholar] [CrossRef] [PubMed]
- Little, M.A.; Smyth, L.; Salama, A.D.; Mukherjee, S.; Smith, J.; Haskard, D.; Nourshargh, S.; Cook, H.T.; Pusey, C.D. Experimental Autoimmune Vasculitis: An Animal Model of Anti-Neutrophil Cytoplasmic Antibody-Associated Systemic Vasculitis. Am. J. Pathol. 2009, 174, 1212–1220. [Google Scholar] [CrossRef] [PubMed]
- Pfister, H.; Ollert, M.; Fröhlich, L.F.; Quintanilla-Martinez, L.; Colby, T.V.; Specks, U.; Jenne, D.E. Antineutrophil Cytoplasmic Autoantibodies Against the Murine Homolog of Proteinase 3 (Wegener Autoantigen) Are Pathogenic In Vivo. Blood 2004, 104, 1411–1418. [Google Scholar] [CrossRef]
- Little, M.A.; Al-Ani, B.; Ren, S.; Al-Nuaimi, H.; Leite, M., Jr.; Alpers, C.E.; Savage, C.O.; Duffield, J.S. Anti-Proteinase 3 Anti-Neutrophil Cytoplasm Autoantibodies Recapitulate Systemic Vasculitis in Mice with a Humanized Immune System. PLoS ONE 2012, 7, e28626. [Google Scholar] [CrossRef]
- Koh, J.H.; Kemna, M.J.; Cohen Tervaert, J.W.; Kim, W.U. Editorial: Can an Increase in Antineutrophil Cytoplasmic Autoantibody Titer Predict Relapses in Antineutrophil Cytoplasmic Antibody-Associated Vasculitis? Arthritis Rheumatol. 2016, 68, 1571–1573. [Google Scholar] [CrossRef]
- Tervaert, J.W.; van der Woude, F.J.; Fauci, A.S.; Ambrus, J.L.; Velosa, J.; Keane, W.F.; Meijer, S.; van der Giessen, M.; van der Hem, G.K.; The, T.H. Association Between Active Wegener’s Granulomatosis and Anticytoplasmic Antibodies. Arch. Intern. Med. 1989, 149, 2461–2465. [Google Scholar] [CrossRef]
- Kemna, M.J.; Damoiseaux, J.; Austen, J.; Winkens, B.; Peters, J.; van Paassen, P.; Cohen Tervaert, J.W. ANCA as a Predictor of Relapse: Useful in Patients with Renal Involvement but Not in Patients with Nonrenal Disease. J. Am. Soc. Nephrol. 2015, 26, 537–542. [Google Scholar] [CrossRef] [PubMed]
- Fussner, L.A.; Hummel, A.M.; Schroeder, D.R.; Silva, F.; Cartin-Ceba, R.; Snyder, M.R.; Hoffman, G.S.; Kallenberg, C.G.; Langford, C.A.; Merkel, P.A.; et al. Factors Determining the Clinical Utility of Serial Measurements of Antineutrophil Cytoplasmic Antibodies Targeting Proteinase 3. Arthritis Rheumatol. 2016, 68, 1700–1710. [Google Scholar] [CrossRef]
- Jones, R.B.; Tervaert, J.W.; Hauser, T.; Luqmani, R.; Morgan, M.D.; Peh, C.A.; Savage, C.O.; Segelmark, M.; Tesar, V.; van Paassen, P.; et al. Rituximab Versus Cyclophosphamide in ANCA-Associated Renal Vasculitis. N. Engl. J. Med. 2010, 363, 211–220. [Google Scholar] [CrossRef] [PubMed]
- Stone, J.H.; Merkel, P.A.; Spiera, R.; Seo, P.; Langford, C.A.; Hoffman, G.S.; Kallenberg, C.G.; St Clair, E.W.; Turkiewicz, A.; Tchao, N.K.; et al. Rituximab Versus Cyclophosphamide for ANCA-Associated Vasculitis. N. Engl. J. Med. 2010, 363, 221–232. [Google Scholar] [CrossRef] [PubMed]
- Specks, U.; Merkel, P.A.; Seo, P.; Spiera, R.; Langford, C.A.; Hoffman, G.S.; Kallenberg, C.G.; St Clair, E.W.; Fessler, B.J.; Ding, L.; et al. Efficacy of Remission-Induction Regimens for ANCA-Associated Vasculitis. N. Engl. J. Med. 2013, 369, 417–427. [Google Scholar] [CrossRef] [PubMed]
- Guillevin, L.; Pagnoux, C.; Karras, A.; Khouatra, C.; Aumaître, O.; Cohen, P.; Maurier, F.; Decaux, O.; Ninet, J.; Gobert, P.; et al. Rituximab versus azathioprine for maintenance in ANCA-associated vasculitis. N. Engl. J. Med. 2014, 371, 1771–1780. [Google Scholar] [CrossRef]
- Stone, J.H.; Merkel, P.A.; Seo, P.; Spiera, R.; Langford, C.A.; Hoffman, G.S. Extended Follow-Up of Treatment with Rituximab Versus Cyclophosphamide for Remission-Induction of ANCA-Associated Vasculitis: Which Subsets Are at Greatest Risk for Flare? Arthritis Rheum. 2011, 63, S946–S947. [Google Scholar]
- Alberici, F.; Smith, R.M.; Jones, R.B.; Roberts, D.M.; Willcocks, L.C.; Chaudhry, A.; Smith, K.G.C.; Jayne, D.R.W. Long-Term Follow-Up of Patients Who Received Repeat-Dose Rituximab as Maintenance Therapy for ANCA-Associated Vasculitis. Rheumatology 2015, 54, 1153–1160. [Google Scholar] [CrossRef]
- Charles, P.; Terrier, B.; Perrodeau, É.; Cohen, P.; Faguer, S.; Huart, A.; Hamidou, M.; Agard, C.; Bonnotte, B.; Samson, M.; 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. [Google Scholar] [CrossRef] [PubMed]
- Bunch, D.O.; Mendoza, C.E.; Aybar, L.T.; Kotzen, E.S.; Colby, K.R.; Hu, Y.; Hogan, S.L.; Poulton, C.J.; Schmitz, J.L.; Falk, R.J.; et al. Relapse Risk from B Cell Phenotype: Decreased CD5+ B Cells Portend a Shorter Time to Relapse After B Cell Depletion in Patients with ANCA-Associated Vasculitis. Ann. Rheum. Dis. 2015, 74, 1784–1786. [Google Scholar] [CrossRef] [PubMed]
- Md Yusof, M.Y.; Vital, E.M.; Das, S.; Dass, S.; Arumugakani, G.; Savic, S.; Rawstron, A.C.; Emery, P. Repeat Cycles of Rituximab on Clinical Relapse in ANCA-Associated Vasculitis: Identifying B Cell Biomarkers for Relapse to Guide Retreatment Decisions. Ann. Rheum. Dis. 2015, 74, 1734–1738. [Google Scholar] [CrossRef] [PubMed]
- Kurz, T.; Weiner, M.; Skoglund, C.; Basnet, S.; Eriksson, P.; Segelmark, M. A Myelopoiesis Gene Signature During Remission in Anti-Neutrophil Cytoplasm Antibody-Associated Vasculitis Does Not Predict Relapses But Seems to Reflect Ongoing Prednisolone Therapy. Clin. Exp. Immunol. 2014, 175, 215–226. [Google Scholar] [CrossRef] [PubMed]
- Bournazos, S.; Ravetch, J.V. Diversification of IgG Effector Functions. Int. Immunol. 2017, 29, 303–310. [Google Scholar] [CrossRef]
- Kemna, M.J.; Plomp, R.; van Paassen, P.; Koeleman, C.A.M.; Jansen, B.C.; Damoiseaux, J.G.M.C.; Cohen Tervaert, J.W.; Wuhrer, M. Galactosylation and Sialylation Levels of IgG Predict Relapse in Patients with PR3-ANCA Associated Vasculitis. eBioMedicine 2017, 17, 108–118. [Google Scholar] [CrossRef]
- Wojcik, I.; Wuhrer, M.; Heeringa, P.; Stegeman, C.A.; Rutgers, A.; Falck, D. Specific IgG Glycosylation Differences Precede Relapse in PR3-ANCA Associated Vasculitis Patients with and Without ANCA Rise. Front. Immunol. 2023, 14, 1214945. [Google Scholar] [CrossRef]
- Prskalo, L.; Skopnik, C.M.; Goerlich, N.; Freund, P.; Wagner, L.; Grothgar, E.; Mirkheshti, P.; Klocke, J.; Sonnemann, J.; Metzke, D.; et al. Urinary CD4+ T Cells Predict Renal Relapse in ANCA-Associated Vasculitis. J. Am. Soc. Nephrol. 2024, 35, 483–494. [Google Scholar] [CrossRef]
- Rhee, R.L.; Davis, J.C.; Ding, L.; Fervenza, F.C.; Hoffman, G.S.; Kallenberg, C.G.M.; Langford, C.A.; McCune, W.J.; Monach, P.A.; Seo, P.; et al. The Utility of Urinalysis in Determining the Risk of Renal Relapse in ANCA-Associated Vasculitis. Clin. J. Am. Soc. Nephrol. 2018, 13, 251–257. [Google Scholar] [CrossRef]
- Lugli, G.; Buscemi, P.; Calatroni, M.; Alderotti, G.; Preciado, F.G.; Moroni, G.L.; Sinico, R.A.; Emmi, G.; Peyronel, F.; Little, M.; et al. Development of a relapse risk score in patients with ANCA-associated vasculitis treated with cyclophosphamide induction. Nephrol. Dial. Transplant. 2024, 39, gfae069.019. [Google Scholar] [CrossRef]
- Samson, M.; Devilliers, H.; Thietart, S.; Charles, P.; Pagnoux, C.; Cohen, P.; Karras, A.; Mouthon, L.; Terrier, B.; Puéchal, X.; et al. Score to assess the probability of relapse in granulomatosis with polyangiitis and microscopic polyangiitis. RMD Open 2023, 9, e002953. [Google Scholar] [CrossRef] [PubMed]
Relapse Predictors | Well Described | Proposed |
---|---|---|
At baseline | antiPR3 presence | CD27+CD38hi B cells |
low-density granulocytes | ||
TNFSF13B rs3759467 (snp) | ||
respiratory tract and cardiovascular involvement | HLA-DPB1*04:01 | |
CCL18 | ||
calprotectin | ||
S. aureus carriage | endothelial progenitor cells (EPCs) | |
sclerotic class glomerulonephritis lack of interstitial infiltrates on renal biopsy | ||
Upon remission | ANCA reappearance | galactosylation and sialyation in IgG1 |
IgG Fc-fucosylation | ||
B cell reconstitution | urinary CD4+ count | |
persisting hematuria |
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2024 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Wawrzycka-Adamczyk, K.; Korkosz, M.; Musiał, J.; Wójcik, K. Relapse Predictors in Antineutrophil Cytoplasmic Antibody (ANCA)-Associated Vasculitis. Diagnostics 2024, 14, 1849. https://doi.org/10.3390/diagnostics14171849
Wawrzycka-Adamczyk K, Korkosz M, Musiał J, Wójcik K. Relapse Predictors in Antineutrophil Cytoplasmic Antibody (ANCA)-Associated Vasculitis. Diagnostics. 2024; 14(17):1849. https://doi.org/10.3390/diagnostics14171849
Chicago/Turabian StyleWawrzycka-Adamczyk, Katarzyna, Mariusz Korkosz, Jacek Musiał, and Krzysztof Wójcik. 2024. "Relapse Predictors in Antineutrophil Cytoplasmic Antibody (ANCA)-Associated Vasculitis" Diagnostics 14, no. 17: 1849. https://doi.org/10.3390/diagnostics14171849