Understanding inflammation in juvenile idiopathic arthritis: How immune biomarkers guide clinical strategies in the systemic onset subtype

European Journal of Immunology

Volumn 46, Issue 9, 2016, Pages 2068-2077

  Swart, Joost F ^a   de Roock, Sytze ^a   Prakken, Berent J ^a  

^a UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

Author keywords

Biomarkers; Classification; Juvenile arthritis; Prognosis; Recurrence

Indexed keywords

ANTINUCLEAR ANTIBODY; C REACTIVE PROTEIN; CALGRANULIN B; CALGRANULIN C; HLA B27 ANTIGEN; INTERLEUKIN 18; MULTIDRUG RESISTANCE ASSOCIATED PROTEIN 8; RHEUMATOID FACTOR;

ALGORITHM; DISEASE ACTIVITY; ERYTHROCYTE SEDIMENTATION RATE; HUMAN; PRACTICE GUIDELINE; PRIORITY JOURNAL; PROGNOSIS; REVIEW; SYSTEMIC JUVENILE IDIOPATHIC ARTHRITIS;

EID: 84985910651     PISSN: 00142980     EISSN: 15214141     Source Type: Journal    
DOI: 10.1002/eji.201546092     Document Type: Review

References (70)

1. Thierry, S., Fautrel, B., Lemelle, I. and Guillemin, F., Prevalence and incidence of juvenile idiopathic arthritis: a systematic review. Jt. Bone Spine 2014. 81: 112–117.
2. Prakken, B., Albani, S. and Martini, A., Juvenile idiopathic arthritis. Lancet 2011. 377: 2138–2149.
3. Beukelman, T., Patkar, N. M., Saag, K. G., Tolleson-Rinehart, S., Cron, R. Q., DeWitt, E. M., Ilowite, N. T. et al., 2011 American College of Rheumatology recommendations for the treatment of juvenile idiopathic arthritis: initiation and safety monitoring of therapeutic agents for the treatment of arthritis and systemic features. Arthritis Care Res. (Hoboken) 2011. 63: 465–482.
4. Klein, A., Kaul, I., Foeldvari, I., Ganser, G., Andreas, U. and Horneff, G., Efficacy and safety of oral and parenteral methotrexate therapy in children with juvenile idiopathic arthritis. An observational study with patients of the German Methotrexate Registry. Arthritis Care Res. 2012. 64: 1349–1356.
5. Petty, R. E., Southwood, T. R., Manners, P., Baum, J., Glass, D. N., Goldenberg, J., He, X. et al., International league of associations for rheumatology classification of juvenile idiopathic arthritis: second revision, Edmonton, 2001. J. Rheumatol. 2004. 31: 390–392.
6. Ravelli, A. and Martini, A., Juvenile idiopathic arthritis. Lancet. 2007. 369: 767–778.
7. De Kleer, I. M., Wedderburn, L. R., Taams, L. S., Patel, A., Varsani, H., Klein, M., de Jager, W. et al., CD4+CD25bright regulatory T cells actively regulate inflammation in the joints of patients with the remitting form of juvenile idiopathic arthritis. J. Immunol. 2004. 172: 6435–6443.
8. Pascual, V., Allantaz, F., Arce, E., Punaro, M. and Banchereau, J., Role of interleukin-1 (IL-1) in the pathogenesis of systemic onset juvenile idiopathic arthritis and clinical response to IL-1 blockade. J. Exp. Med. 2005. 201: 1479–1486.
9. Guzman, J., Burgos-Vargas, R., Duarte-Salazar, C. and Gomez-Mora, P., Reliability of the articular examination in children with juvenile rheumatoid arthritis: interobserver agreement and sources of disagreement. J. Rheumatol. 1995. 22: 2331–2336.
10. Şenocak, Ö̈., Ünsal, E., Akalin, E. and Ergör, G., Interobserver reliability of articular examination in juvenile idiopathic arthritis. Turk. J. Pediatr. 2003. 45: 29–32.
11. Magni-Manzoni, S., Epis, O., Ravelli, A., Klersy, C., Visconti, C., Lanni, S., Muratore, V. et al., Comparison of clinical versus ultrasound-determined synovitis in juvenile idiopathic arthritis. Arthritis Care Res. 2009. 61: 1497–1504. DOI: 10.1002/art.24823.
12. Magni-Manzoni, S., Scirè, C. A., Ravelli, A., Klersy, C., Rossi, S., Muratore, V., Visconti, C. et al., Ultrasound-detected synovial abnormalities are frequent in clinically inactive juvenile idiopathic arthritis, but do not predict a flare of synovitis. Ann. Rheum. Dis. 2013. 72: 223–228.
13. Petty, R. and Southwood, T., International League of Associations for Rheumatology classification of juvenile idiopathic arthritis: second revision, Edmonton, 2001. Rheumatol. 2004. 31: 390–392.
14. Schneider, R. and Passo, M. H., Juvenile rheumatoid arthritis. Rheum. Dis. Clin. North Am. 2002. 28: 503–530.
15. Martini, A., It is time to rethink juvenile idiopathic arthritis classification and nomenclature. Ann. Rheum. Dis. 2012. 71: 1437–1439.
16. Strimbu, K. and Tavel, J. A., NIH public access. Curr. Opin. HIV AIDS. 2011. 5: 463–466.
17. Definitions, B. and Group, W., Biomarkers and surrogate endpoints: preferred definitions and conceptual framework. Clin. Pharmacol. Ther. 2001. 69: 89–95.
18. Stoll, M. L., Bhore, R., Dempsey-Robertson, M. and Punaro, M., Spondyloarthritis in a pediatric population: risk factors for sacroiliitis. J. Rheumatol. 2010. 37: 2402–2408.
19. Lin, C., MacKenzie, J. D., Courtier, J. L., Gu, J. T. and Milojevic, D., Magnetic resonance imaging findings in juvenile spondyloarthropathy and effects of treatment observed on subsequent imaging. Pediatr. Rheumatol. Online J. 2014. 12: 25.
20. Wallace, C. A., Giannini, E. H., Spalding, S. J., Hashkes, P. J., O'Neil, K. M., Zeft, A. S., Szer, I. S. et al., Trial of early aggressive therapy in polyarticular juvenile idiopathic arthritis. Arthritis Rheum. 2012. 64: 2012–2021.
21. Tynjälä, P., Vähäsalo, P., Tarkiainen, M., Kröger, L., Aalto, K., Malin, M., Putto-Laurila, A. et al., Aggressive combination drug therapy in very early polyarticular juvenile idiopathic arthritis (ACUTE-JIA): a multicentre randomised open-label clinical trial. Ann. Rheum. Dis. 2011. 70: 1605–1612.
22. Van de Stadt, L. A., Witte, B. I., Bos, W. H. and van Schaardenburg, D., A prediction rule for the development of arthritis in seropositive arthralgia patients. Ann. Rheum. Dis. 2013. 72: 1920–1926.
23. Krabben, A., Stomp, W., van der Heijde, D. M. F. M., van Nies, J. A. B., Bloem, J. L., Huizinga, T. W. J., Reijnierse, M. et al., MRI of hand and foot joints of patients with anticitrullinated peptide antibody positive arthralgia without clinical arthritis. Ann. Rheum. Dis. 2013. 72: 1540–1544.
24. Gonzalez-Lopez, L., Gamez-Nava, J. I., Jhangri, G., Russell, A. S. and Suarez-Almazor, M. E., Decreased progression to rheumatoid arthritis or other connective tissue diseases in patients with palindromic rheumatism treated with antimalarials. J. Rheumatol. 2000. 27: 41–46.
25. Tzaribachev, N., Weber, D. and Horger, M., Juvenile idiopathic arthritis: the silent killer of pediatric temporomandibular joints. J. Rheumatol. 2010. 69: 124–129.
26. Aksentijevich, I., Masters, S. L., Ferguson, P. J., Dancey, P., Frenkel, J., van Royen-Kerkhoff, A., Laxer, R. et al., An autoinflammatory disease with deficiency of the interleukin-1-receptor antagonist. N. Engl. J. Med. 2009. 360: 2426–2437.
27. Lomater, C., Gerloni, V., Gattinara, M., Mazzotti, J., Cimaz, R. and Fantini, F., Systemic onset juvenile idiopathic arthritis: a retrospective study of 80 consecutive patients followed for 10 years. J. Rheumatol. 2000. 27: 491–496.
28. Behrens, E. M., Beukelman, T., Paessler, M. and Cron, R. Q., Occult macrophage activation syndrome in patients with systemic juvenile idiopathic arthritis. J. Rheumatol. 2007. 34: 1133–1138.
29. Ravelli, A., Minoia, F., Davì, S., Horne, A., Bovis, F., Pistorio, A., Aricò, M. et al., 2016 classification criteria for macrophage activation syndrome complicating systemic juvenile idiopathic arthritis: a European league against rheumatism/American college of rheumatology/paediatric rheumatology international trials organisation collaborat. Arthritis Rheumatol. 2016. 68: 566–576.
30. Minoia, F., Davì, S., Horne, A., Demirkaya, E., Bovis, F., Li, C., Lehmberg, K. et al., Clinical features, treatment, and outcome of macrophage activation syndrome complicating systemic juvenile idiopathic arthritis: a multinational, multicenter study of 362 patients. Arthritis Rheumatol. 2014. 66: 3160–3169.
31. Pascual, V., Allantaz, F., Arce, E., Punaro, M. and Banchereau, J., Role of interleukin-1 (IL-1) in the pathogenesis of systemic onset juvenile idiopathic arthritis and clinical response to IL-1 blockade. J. Exp. Med. 2005. 201: 1479–1486.
32. Vogl, T., Tenbrock, K., Ludwig, S., Leukert, N., Ehrhardt, C., van Zoelen, M. A. D., Nacken, W. et al., Mrp8 and Mrp14 are endogenous activators of Toll-like receptor 4, promoting lethal, endotoxin-induced shock. Nat. Med. 2007. 13: 1042–1049.
33. Loser, K., Vogl, T., Voskort, M., Lueken, A., Kupas, V., Nacken, W., Klenner, L. et al., The Toll-like receptor 4 ligands Mrp8 and Mrp14 are crucial in the development of autoreactive CD8+ T cells. Nat. Med. 2010. 16: 713–717.
34. Austermann, J., Friesenhagen, J., Fassl, S., Ortkras, T., Burgmann, J., Barczyk-Kahlert, K., Faist, E. et al., Alarmins MRP8 and MRP14 induce stress tolerance in phagocytes under sterile inflammatory conditions. Cell Rep. 2014. 9: 2112–2124.
35. Frosch, M., Ahlmann, M., Vogl, T., Wittkowski, H., Wulffraat, N., Foell, D., Roth, J. et al., The myeloid-related proteins 8 and 14 complex, a novel ligand of toll-like receptor 4, and interleukin-1β form a positive feedback mechanism in systemic-onset juvenile idiopathic arthritis. Arthritis Rheum. 2009. 60: 883–891.
36. Holzinger, D., Frosch, M., Kastrup, A., Prince, F. H. M., Otten, M. H., Van Suijlekom-Smit, L. W. A., ten Cate, R. et al., The Toll-like receptor 4 agonist MRP8/14 protein complex is a sensitive indicator for disease activity and predicts relapses in systemic-onset juvenile idiopathic arthritis. Ann. Rheum. Dis. 2012. 71: 974–980.
37. De Jager, W., Hoppenreijs, E. P. A. H., Wulffraat, N. M., Wedderburn, L. R., Kuis, W. and Prakken, B. J., Blood and synovial fluid cytokine signatures in patients with juvenile idiopathic arthritis: a cross-sectional study. Ann. Rheum. Dis. 2007. 66: 589–598.
38. Shimizu, M., Nakagishi, Y., Inoue, N., Mizuta, M., Ko, G., Saikawa, Y., Kubota, T. et al., Interleukin-18 for predicting the development of macrophage activation syndrome in systemic juvenile idiopathic arthritis. Clin. Immunol. 2015. 160: 277–281.
39. Vastert, S. J., de Jager, W., Noordman, B. J., Holzinger, D., Kuis, W., Prakken, B. J., Wulffraat, N. M. et al., Effectiveness of first-line treatment with recombinant interleukin-1 receptor antagonist in steroid-naive patients with new-onset systemic juvenile idiopathic arthritis: results of a prospective cohort study. Arthritis Rheumatol. (Hoboken, N.J.). 2014. 66: 1034–1043.
40. Flato, B., Hoffmann-Vold, A. M., Reiff, A., Forre, O., Lien, G. and Vinje, O., Long-term outcome and prognostic factors in enthesitis-related arthritis: a case-control study. Arthritis Rheum. 2006. 54: 3573–3582.
41. Van der Linden, S. M., Valkenburg, H. A., de Jongh, B. M. and Cats, A., The risk of developing ankylosing spondylitis in HLA-B27 positive individuals. A comparison of relatives of spondylitis patients with the general population. Arthritis Rheum. 1984. 27: 241–249.
42. Colbert, R. A., DeLay, M. L., Klenk, E. I. and Layh-Schmitt, G., From HLA-B27 to spondyloarthritis: a journey through the ER. Immunol. Rev. 2010. 233: 181–202.
43. Bird, L. A., Peh, C. A., Kollnbeger, S., Elliott, T., McMichael, A. J. A. J. and Bowness, P., Lymphoblastoid cells express HLA-B27 homodimers both intracellularly and at the cell surface following endosomal recycling. Eur. J. Immunol. 2003. 33: 748–759.
44. Berntson, L., Nordal, E., Aalto, K., Peltoniemi, S., Herlin, T., Zak, M., Nielsen, S. et al., HLA-B27 predicts a more chronic disease course in an 8-year followup cohort of patients with juvenile idiopathic arthritis. J. Rheumatol. 2013. 40: 725–731.
45. Arend, W. P. and Firestein, G. S., Pre-rheumatoid arthritis: predisposition and transition to clinical synovitis. Nat. Rev. Rheumatol. 2012. 8: 573–586.
46. Khalkhali-Ellis, Z., Bulla, G. A., Schlesinger, L. S., Kirschmann, D. A., Moore, T. L. and Hendrix, M. J., C1q-containing immune complexes purified from sera of juvenile rheumatoid arthritis patients mediate IL-8 production by human synoviocytes: role of C1q receptors. J. Immunol. 1999. 163: 4612–4620.
47. Vossenaar, E. R.and van Venrooij, W. J., Citrullinated proteins: sparks that may ignite the fire in rheumatoid arthritis. Arthritis Res. Ther. 2004. 6: 107–111.
48. Wang, Y., Pei, F., Wang, X., Sun, Z., Hu, C. and Dou, H., Meta-analysis: diagnostic accuracy of anti-cyclic citrullinated peptide antibody for juvenile idiopathic arthritis. J. Immunol. Res. 2015. 2015: 915276.
49. Agmon-Levin, N., Damoiseaux, J., Kallenberg, C., Sack, U., Witte, T., Herold, M., Bossuyt, X. et al., International recommendations for the assessment of autoantibodies to cellular antigens referred to as anti-nuclear antibodies. Ann. Rheum. Dis. 2014. 73: 17–23.
50. Barnett, E. V., North, A. F. J., Condemi, J. J., Jacox, R. F. and Vaughan, J. H., Antinuclear factors in systemic lupus erythematosus and rheumatoid arthritis. Ann. Intern. Med. 1965. 63: 100–108.
51. Wananukul, S., Voramethkul, W., Kaewopas, Y. and Hanvivatvong, O., Prevalence of positive antinuclear antibodies in healthy children. Asian Pacific J. Allergy Immunol. 2005. 23: 153–157.
52. Malleson, P. N., Sailer, M. and Mackinnon, M. J., Usefulness of antinuclear antibody testing to screen for rheumatic diseases. Arch. Dis. Child. 1997. 77: 299–304.
53. Deane, P. M., Liard, G., Siegel, D. M. and Baum, J., The outcome of children referred to a pediatric rheumatology clinic with a positive antinuclear antibody test but without an autoimmune disease. Pediatrics 1995. 95: 892–895.
54. Ravelli, A., Varnier, G. C., Oliveira, S., Castell, E., Arguedas, O., Magnani, A., Pistorio, A. et al., Antinuclear antibody-positive patients should be grouped as a separate category in the classification of juvenile idiopathic arthritis. Arthritis Rheum. 2011. 63: 267–275.
55. Van den Broek, T., Hoppenreijs, E., Meerding, J., Scholman, R., Otten, H. G., Swart, J. F., Martini, A. et al., Cytokine profiling at disease onset: support for classification of young antinuclear antibody-positive patients as a separate category of juvenile idiopathic arthritis. Ann. Rheum. Dis. 2014. 74: 470–472.
56. Ma, X., Xin, L., Sun, J. and Liu, Z., Antinuclear antibody-positive cohort constitutes homogeneous entity in juvenile idiopathic arthritis. Mod. Rheumatol. 2015. 7595: 1–5.
57. Gilliam, B. E., Chauhan, A. K., Low, J. M. and Moore, T. L., Measurement of biomarkers in juvenile idiopathic arthritis patients and their significant association with disease severity: a comparative study. Clin. Exp. Rheumatol. 2008. 26: 492–497.
58. Flato, B., Lien, G., Smerdel, A., Vinje, O., Dale, K., Johnston, V., Sorskaar, D. et al., Prognostic factors in juvenile rheumatoid arthritis: a case-control study revealing early predictors and outcome after 14.9 years. J. Rheumatol. 2003. 30: 386–393.
59. Flato, B., Aasland, A., Vinje, O. and Forre, O., Outcome and predictive factors in juvenile rheumatoid arthritis and juvenile spondyloarthropathy. J.Rheumatol. 1998. 25: 366–375.
60. Guillaume, S., Prieur, A. M., Coste, J. and Job-Deslandre, C., Long-term outcome and prognosis in oligoarticular-onset juvenile idiopathic arthritis. Arthritis Rheum. 2000. 43: 1858–1865.
61. Consolaro, A., Ruperto, N., Bazso, A., Pistorio, A., Magni-Manzoni, S., Filocamo, G., Malattia, C. et al., Development and validation of a composite disease activity score for juvenile idiopathic arthritis. Arthritis Rheum. 2009. 61: 658–666.
62. Consolaro, A., Negro, G., Lanni, S., Solari, N., Martini, A. and Ravelli, A., Toward a treat-to-target approach in the management of juvenile idiopathic arthritis. Clin. Exp. Rheumatol. 2012. 30: S157–S162.
63. Frosch, M., Strey, A., Vogl, T., Wulffraat, N. M., Kuis, W., Sunderkötter, C., Harms, E. et al., Myeloid-related proteins 8 and 14 are specifically secreted during interaction of phagocytes and activated endothelium and are useful markers for monitoring disease activity in pauciarticular-onset juvenile rheumatoid arthritis. Arthritis Rheum. 2000. 43: 628–637.
64. Foell, D., Wittkowski, H., Hammerschmidt, I., Wulffraat, N., Schmeling, H., Frosch, M., Horneff, G. et al., Monitoring neutrophil activation in juvenile rheumatoid arthritis by S100A12 serum concentrations. Arthritis Rheum. 2004. 50: 1286–1295.
65. Moncrieffe, H., Ursu, S., Holzinger, D., Patrick, F., Kassoumeri, L., Wade, A., Roth, J. et al., A subgroup of juvenile idiopathic arthritis patients who respond well to methotrexate are identified by the serum biomarker MRP8/14 protein. Rheumatology 2013. 52: 1467–1476.
66. Kahn, R., Berthold, E., Gullstrand, B., Schmidt, T., Kahn, F., Geborek, P., Saxne, T. et al., Circulating complexes between tumour necrosis factor-alpha and etanercept predict long-term efficacy of etanercept in juvenile idiopathic arthritis. Acta Paediatr. Int. J. Paediatr. 2016. 105: 427–432.
67. Gerss, J., Roth, J., Holzinger, D., Ruperto, N., Wittkowski, H., Frosch, M., Wulffraat, N. et al., Phagocyte-specific S100 proteins and high-sensitivity C reactive protein as biomarkers for a risk-adapted treatment to maintain remission in juvenile idiopathic arthritis: a comparative study. Ann. Rheum. Dis. 2012. 71: 1991–1997.
68. Yamasaki, Y., Takei, S., Imanaka, H., Nerome, Y., Kubota, T., Nonaka, Y., Akaike, H. et al., Prediction of long-term remission of oligo/polyarticular juvenile idiopathic arthritis with S100A12 and Vascular Endothelial Growth Factor. Mod. Rheumatol. 2015. 7595: 1–23.
69. Anink, J., Van Suijlekom-Smit, L. W. A., Otten, M. H., Prince, F. H. M., van Rossum, M. A. J., Dolman, K. M., Hoppenreijs, E. P. A. H. et al., MRP8/14 serum levels as a predictor of response to starting and stopping anti-TNF treatment in juvenile idiopathic arthritis. Arthritis Res. Ther. 2015. 17: 200–207.
70. Rothmund, F., Gerss, J., Ruperto, N., Däbritz, J., Wittkowski, H., Frosch, M., Wulffraat, N. M. et al., Validation of relapse risk biomarkers for routine use in patients with juvenile idiopathic arthritis. Arthritis Care Res. (Hoboken). 2014. 66: 949–955.