Review: The preclinical phase of rheumatoid arthritis: What is acknowledged and what needs to be assessed?

Arthritis and Rheumatism

Volumn 65, Issue 9, 2013, Pages 2219-2232

  Van Steenbergen, H W ^a   Huizinga, T W J ^a   Van Der Helm Van Mil, A H M ^a  

^a LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

AUTOANTIBODY; BIOLOGICAL MARKER; C REACTIVE PROTEIN; CITRULLINATED PROTEIN ANTIBODY; LIPID; RHEUMATOID FACTOR; UNCLASSIFIED DRUG; ANTIRHEUMATIC AGENT;

ARTHRALGIA; AUTOIMMUNITY; BONE METABOLISM; CARDIOVASCULAR DISEASE; CARDIOVASCULAR RISK; CLINICAL FEATURE; COHORT ANALYSIS; DISEASE COURSE; ENVIRONMENTAL FACTOR; GENETIC RISK; HUMAN; INFLAMMATION; LONGITUDINAL STUDY; NUCLEAR MAGNETIC RESONANCE IMAGING; POSITRON EMISSION TOMOGRAPHY; PRIORITY JOURNAL; PROGNOSIS; REVIEW; RHEUMATOID ARTHRITIS; RISK FACTOR; SMOKING; ARTICLE; GENETICS; PRODROMAL SYMPTOM; ARTHRITIS, RHEUMATOID;

ANTIRHEUMATIC AGENTS; ARTHRITIS, RHEUMATOID; HUMANS; PRODROMAL SYMPTOMS; RISK FACTORS;

EID: 84883220450     PISSN: 00043591     EISSN: 15290131     Source Type: Journal    
DOI: 10.1002/art.38013     Document Type: Review

References (63)

1. Finckh A, Liang MH, van Herckenrode CM, de Pablo P,. Long-term impact of early treatment on radiographic progression in rheumatoid arthritis: a meta-analysis. Arthritis Rheum 2006; 55: 864-72.
2. Van der Linden MP, le Cessie S, Raza K, van der Woude D, Knevel R, Huizinga TW, et al. Long-term impact of delay in assessment of patients with early arthritis. Arthritis Rheum 2010; 62: 3537-46.
3. Aho K, Palosuo T, Raunio V, Puska P, Aromaa A, Salonen JT,. When does rheumatoid disease start? Arthritis Rheum 1985; 28: 485-9.
4. Jonsson T, Thorsteinsson J, Kolbeinsson A, Jonasdottir E, Sigfusson N, Valdimarsson H,. Population study of the importance of rheumatoid factor isotypes in adults. Ann Rheum Dis 1992; 51: 863-8.
5. Aho K, von Essen R, Kurki P, Palosuo T, Heliovaara M,. Antikeratin antibody and antiperinuclear factor as markers for subclinical rheumatoid disease process. J Rheumatol 1993; 20: 1278-81.
6. Kurki P, Aho K, Palosuo T, Heliovaara M,. Immunopathology of rheumatoid arthritis: antikeratin antibodies precede the clinical disease. Arthritis Rheum 1992; 35: 914-7.
7. Del Puente A, Knowler WC, Pettitt DJ, Bennett PH,. The incidence of rheumatoid arthritis is predicted by rheumatoid factor titer in a longitudinal population study. Arthritis Rheum 1988; 31: 1239-44.
8. Walker DJ, Pound JD, Griffiths ID, Powell RJ,. Rheumatoid factor tests in the diagnosis and prediction of rheumatoid arthritis. Ann Rheum Dis 1986; 45: 684-90.
9. Silman AJ, Hennessy E, Ollier B,. Incidence of rheumatoid arthritis in a genetically predisposed population. Br J Rheumatol 1992; 31: 365-8.
10. Rantapaa-Dahlqvist S, de Jong BA, Berglin E, Hallmans G, Wadell G, Stenlund H, et al. Antibodies against cyclic citrullinated peptide and IgA rheumatoid factor predict the development of rheumatoid arthritis. Arthritis Rheum 2003; 48: 2741-9.
11. Nielen MM, van Schaardenburg D, Reesink HW, van de Stadt RJ, van der Horst-Bruinsma IE, de Koning MH, et al. Specific autoantibodies precede the symptoms of rheumatoid arthritis: a study of serial measurements in blood donors. Arthritis Rheum 2004; 50: 380-6.
12. Gerlag DM, Raza K, van Baarsen LG, Brouwer E, Buckley CD, Burmester GR, et al. EULAR recommendations for terminology and research in individuals at risk of rheumatoid arthritis: report from the Study Group for Risk Factors for Rheumatoid Arthritis. Ann Rheum Dis 2012; 71: 638-41.
13. Van der Woude D, Houwing-Duistermaat JJ, Toes RE, Huizinga TW, Thomson W, Worthington J, et al. Quantitative heritability of anti-citrullinated protein antibody-positive and anti-citrullinated protein antibody-negative rheumatoid arthritis. Arthritis Rheum 2009; 60: 916-23.
14. Hoovestol RA, Mikuls TR,. Environmental exposures and rheumatoid arthritis risk. Curr Rheumatol Rep 2011; 13: 431-9.
15. Lahiri M, Morgan C, Symmons DP, Bruce IN,. Modifiable risk factors for RA: prevention, better than cure? Rheumatology (Oxford) 2012; 51: 499-512.
16. Klareskog L, Stolt P, Lundberg K, Kallberg H, Bengtsson C, Grunewald J, et al and the Epidemiological Investigation of Rheumatoid Arthritis Study Group. A new model for an etiology of rheumatoid arthritis: smoking may trigger HLA-DR (shared epitope)-restricted immune reactions to autoantigens modified by citrullination. Arthritis Rheum 2006; 54: 38-46.
17. Keenan BT, Chibnik LB, Cui J, Ding B, Padyukov L, Kallberg H, et al. Effect of interactions of glutathione S-transferase T1, M1, and P1 and HMOX1 gene promoter polymorphisms with heavy smoking on the risk of rheumatoid arthritis. Arthritis Rheum 2010; 62: 3196-210.
18. Jorgensen KT, Wiik A, Pedersen M, Hedegaard CJ, Vestergaard BF, Gislefoss RE, et al. Cytokines, autoantibodies and viral antibodies in premorbid and postdiagnostic sera from patients with rheumatoid arthritis: case-control study nested in a cohort of Norwegian blood donors. Ann Rheum Dis 2008; 67: 860-6.
19. Kokkonen H, Soderstrom I, Rocklov J, Hallmans G, Lejon K, Rantapaa Dahlqvist S,. Up-regulation of cytokines and chemokines predates the onset of rheumatoid arthritis. Arthritis Rheum 2010; 62: 383-91.
20. Shadick NA, Cook NR, Karlson EW, Ridker PM, Maher NE, Manson JE, et al. C-reactive protein in the prediction of rheumatoid arthritis in women. Arch Intern Med 2006; 166: 2490-4.
21. Turesson C, Bergstrom U, Jacobsson LT, Truedsson L, Berglund G, Saxne T,. Increased cartilage turnover and circulating autoantibodies in different subsets before the clinical onset of rheumatoid arthritis. Ann Rheum Dis 2011; 70: 520-2.
22. Majka DS, Deane KD, Parrish LA, Lazar AA, Baron AE, Walker CW, et al. Duration of preclinical rheumatoid arthritis-related autoantibody positivity increases in subjects with older age at time of disease diagnosis. Ann Rheum Dis 2008; 67: 801-7.
23. Chibnik LB, Mandl LA, Costenbader KH, Schur PH, Karlson EW,. Comparison of threshold cutpoints and continuous measures of anti-cyclic citrullinated peptide antibodies in predicting future rheumatoid arthritis. J Rheumatol 2009; 36: 706-11.
24. Sokolove J, Bromberg R, Deane KD, Lahey LJ, Derber LA, Chandra PE, et al. Autoantibody epitope spreading in the pre-clinical phase predicts progression to rheumatoid arthritis. PLoS One 2012; 7: e35296.
25. Van der Woude D, Rantapaa-Dahlqvist S, Ioan-Facsinay A, Onnekink C, Schwarte CM, Verpoort KN, et al. Epitope spreading of the anti-citrullinated protein antibody response occurs before disease onset and is associated with the disease course of early arthritis. Ann Rheum Dis 2010; 69: 1554-61.
26. Van de Stadt LA, de Koning MH, van de Stadt RJ, Wolbink G, Dijkmans BA, Hamann D, et al. Development of the anti-citrullinated protein antibody repertoire prior to the onset of rheumatoid arthritis. Arthritis Rheum 2011; 63: 3226-33.
27. Masi AT, Aldag JC, Sipes J,. Do elevated levels of serum C-reactive protein predict rheumatoid arthritis in men: correlations with pre-RA status and baseline positive rheumatoid factors. J Rheumatol 2001; 28: 2359-61.
28. Aho K, Palosuo T, Knekt P, Alha P, Aromaa A, Heliovaara M,. Serum C-reactive protein does not predict rheumatoid arthritis. J Rheumatol 2000; 27: 1136-8.
29. Rantapaa-Dahlqvist S, Boman K, Tarkowski A, Hallmans G,. Up regulation of monocyte chemoattractant protein-1 expression in anti-citrulline antibody and immunoglobulin M rheumatoid factor positive subjects precedes onset of inflammatory response and development of overt rheumatoid arthritis. Ann Rheum Dis 2007; 66: 121-3.
30. Karlson EW, Chibnik LB, Tworoger SS, Lee IM, Buring JE, Shadick NA, et al. Biomarkers of inflammation and development of rheumatoid arthritis in women from two prospective cohort studies. Arthritis Rheum 2009; 60: 641-52.
31. Deane KD, O'Donnell CI, Hueber W, Majka DS, Lazar AA, Derber LA, et al. The number of elevated cytokines and chemokines in preclinical seropositive rheumatoid arthritis predicts time to diagnosis in an age-dependent manner. Arthritis Rheum 2010; 62: 3161-72.
32. Nielen MM, van Schaardenburg D, Reesink HW, Twisk JW, van de Stadt RJ, van der Horst-Bruinsma IE, et al. Increased levels of C-reactive protein in serum from blood donors before the onset of rheumatoid arthritis. Arthritis Rheum 2004; 50: 2423-7.
33. Kokkonen H, Mullazehi M, Berglin E, Hallmans G, Wadell G, Ronnelid J, et al. Antibodies of IgG, IgA and IgM isotypes against cyclic citrullinated peptide precede the development of rheumatoid arthritis. Arthritis Res Ther 2011; 13: R13.
34. Nielen MM, van Schaardenburg D, Reesink HW, Twisk JW, van de Stadt RJ, van der Horst-Bruinsma IE, et al. Simultaneous development of acute phase response and autoantibodies in preclinical rheumatoid arthritis. Ann Rheum Dis 2006; 65: 535-7.
35. Van Schaardenburg D, Nielen MM, Lems WF, Twisk JW, Reesink HW, van de Stadt RJ, et al. Bone metabolism is altered in preclinical rheumatoid arthritis. Ann Rheum Dis 2011; 70: 1173-4.
36. Van Halm VP, Nielen MM, Nurmohamed MT, van Schaardenburg D, Reesink HW, Voskuyl AE, et al. Lipids and inflammation: serial measurements of the lipid profile of blood donors who later developed rheumatoid arthritis. Ann Rheum Dis 2007; 66: 184-8.
37. Myasoedova E, Crowson CS, Kremers HM, Fitz-Gibbon PD, Therneau TM, Gabriel SE,. Total cholesterol and LDL levels decrease before rheumatoid arthritis. Ann Rheum Dis 2010; 69: 1310-4.
38. Maradit-Kremers H, Crowson CS, Nicola PJ, Ballman KV, Roger VL, Jacobsen SJ, et al. Increased unrecognized coronary heart disease and sudden deaths in rheumatoid arthritis: a population-based cohort study. Arthritis Rheum 2005; 52: 402-11.
39. Holmqvist ME, Wedren S, Jacobsson LT, Klareskog L, Nyberg F, Rantapaa-Dahlqvist S, et al. No increased occurrence of ischemic heart disease prior to the onset of rheumatoid arthritis: results from two Swedish population-based rheumatoid arthritis cohorts. Arthritis Rheum 2009; 60: 2861-9.
40. Kerola AM, Kerola T, Kauppi MJ, Kautiainen H, Virta LJ, Puolakka K, et al. Cardiovascular comorbidities antedating the diagnosis of rheumatoid arthritis. Ann Rheum Dis 2012. E-pub ahead of print.
41. Bos WH, Wolbink GJ, Boers M, Tijhuis GJ, de Vries N, van der Horst-Bruinsma IE, et al. Arthritis development in patients with arthralgia is strongly associated with anti-citrullinated protein antibody status: a prospective cohort study. Ann Rheum Dis 2010; 69: 490-4.
42. Van Baarsen LG, Bos WH, Rustenburg F, van der Pouw Kraan TC, Wolbink GJ, Dijkmans BA, et al. Gene expression profiling in autoantibody-positive patients with arthralgia predicts development of arthritis. Arthritis Rheum 2010; 62: 694-704.
43. Van de Sande MG, de Hair MJ, van der Leij C, Klarenbeek PL, Bos WH, Smith MD, et al. Different stages of rheumatoid arthritis: features of the synovium in the preclinical phase. Ann Rheum Dis 2011; 70: 772-7.
44. Van de Stadt LA, Bos WH, Meursinge RM, Wieringa H, Turkstra F, van der Laken CJ, et al. The value of ultrasonography in predicting arthritis in auto-antibody positive arthralgia patients: a prospective cohort study. Arthritis Res Ther 2010; 12: R98.
45. Van de Stadt LA, van der Horst AR, de Koning MH, Bos WH, Wolbink GJ, van de Stadt RJ, et al. The extent of the anti-citrullinated protein antibody repertoire is associated with arthritis development in patients with seropositive arthralgia. Ann Rheum Dis 2011; 70: 128-33.
46. Gent YY, Voskuyl AE, Kloet RW, van Schaardenburg D, Hoekstra OS, Dijkmans BA, et al. Macrophage positron emission tomography imaging as a biomarker for preclinical rheumatoid arthritis: findings of a prospective pilot study. Arthritis Rheum 2012; 64: 62-6.
47. Limper M, van de Stadt L, Bos W, de Kruif M, Spek A, Wolbink G, et al. The acute-phase response is not predictive for the development of arthritis in seropositive arthralgia-a prospective cohort study. J Rheumatol 2012; 39: 1914-7.
48. Van de Stadt LA, van Sijl AM, van Schaardenberg D, Nurmohamed MT,. Dyslipidaemia in patients with seropositive arthralgia predicts the development of arthritis. Ann Rheum Dis 2012; 71: 1915-6.
49. De Hair MJ, Landewe RB, van de Sande MG, van Schaardenburg D, van Baarsen LG, Gerlag DM, et al. Smoking and overweight determine the likelihood of developing rheumatoid arthritis. Ann Rheum Dis 2012. E-pub ahead of print.
50. Kraan MC, Versendaal H, Jonker M, Bresnihan B, Post WJ, 't Hart BA, et al. Asymptomatic synovitis precedes clinically manifest arthritis. Arthritis Rheum 1998; 41: 1481-8.
51. Krabben A, Stomp W, van der Heijde DM, van Nies JA, Bloem HL, Huizinga TW, et al. MRI of hand and foot joints of patients with anticitrullinated peptide antibody positive arthralgia without clinical arthritis. Ann Rheum Dis 2013. E-pub ahead of print.
52. Hitchon CA, Chandad F, Ferucci ED, Willemze A, Ioan-Facsinay A, van der Woude D, et al. Antibodies to porphyromonas gingivalis are associated with anticitrullinated protein antibodies in patients with rheumatoid arthritis and their relatives. J Rheumatol 2010; 37: 1105-12.
53. Mikuls TR, Thiele GM, Deane KD, Payne JB, O'Dell JR, Yu F, et al. Porphyromonas gingivalis and disease-related autoantibodies in individuals at increased risk of rheumatoid arthritis. Arthritis Rheum 2012; 64: 3522-30.
54. Demoruelle MK, Weisman MH, Simonian PL, Lynch DA, Sachs PB, Pedraza IF, et al. Airways abnormalities and rheumatoid arthritis-related autoantibodies in subjects without arthritis: early injury or initiating site of autoimmunity? Arthritis Rheum 2012; 64: 1756-61.
55. Harre U, Georgess D, Bang H, Bozec A, Axmann R, Ossipova E, et al. Induction of osteoclastogenesis and bone loss by human autoantibodies against citrullinated vimentin. J Clin Invest 2012; 122: 1791-802.
56. Liang KP, Kremers HM, Crowson CS, Snyder MR, Therneau TM, Roger VL, et al. Autoantibodies and the risk of cardiovascular events. J Rheumatol 2009; 36: 2462-9.
57. Bos WH, Dijkmans BA, Boers M, van de Stadt RJ, van Schaardenburg D,. Effect of dexamethasone on autoantibody levels and arthritis development in patients with arthralgia: a randomised trial. Ann Rheum Dis 2010; 69: 571-4.
58. Kolfenbach JR, Deane KD, Derber LA, O'Donnell C, Weisman MH, Buckner JH, et al. A prospective approach to investigating the natural history of preclinical rheumatoid arthritis (RA) using first-degree relatives of probands with RA. Arthritis Rheum 2009; 61: 1735-42.
59. El-Gabalawy HS, Robinson DB, Hart D, Elias B, Markland J, Peschken CA, et al. Immunogenetic risks of anti-cyclical citrullinated peptide antibodies in a North American Native population with rheumatoid arthritis and their first-degree relatives. J Rheumatol 2009; 36: 1130-5.
60. El-Gabalawy HS, Robinson DB, Smolik I, Hart D, Elias B, Wong K, et al. Familial clustering of the serum cytokine profile in the relatives of rheumatoid arthritis patients. Arthritis Rheum 2012; 64: 1720-9.
61. Hughes-Austin JM, Deane KD, Derber LA, Kolfenbach JR, Zerbe GO, Sokolove J, et al. Multiple cytokines and chemokines are associated with rheumatoid arthritis-related autoimmunity in first-degree relatives without rheumatoid arthritis: Studies of the Aetiology of Rheumatoid Arthritis (SERA). Ann Rheum Dis 2013; 72: 901-7.
62. Kolfenbach JR, Deane KD, Derber LA, O'Donnell CI, Gilliland WR, Edison JD, et al. Autoimmunity to peptidyl arginine deiminase type 4 precedes clinical onset of rheumatoid arthritis. Arthritis Rheum 2010; 62: 2633-9.
63. Van de Stadt LA, Witte BI, Bos WH, van Schaardenburg D,. A prediction rule for the development of arthritis in seropositive arthralgia patients. Ann Rheum Dis 2012. E-pub ahead of print.