Review: Preclinical Rheumatoid Arthritis Progress Toward Prevention

Arthritis and Rheumatology

Volumn 68, Issue 4, 2016, Pages 779-788

  Mankia, Kulveer ^a   Emery, Paul ^a  

^a UNIVERSITY OF LEEDS   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

AUTOANTIBODY; CYCLIC CITRULLINATED PEPTIDE ANTIBODY; PROTEIN ARGININE DEIMINASE; RHEUMATOID FACTOR; ANTIRHEUMATIC AGENT; AVIAN PROTEIN; CYTOKINE; EMF-1 PROTEIN, GALLUS GALLUS; HLA DRB1 ANTIGEN;

ARTICLE; AUTOIMMUNITY; BONE MARROW EDEMA; CLINICAL FEATURE; DISEASE CLASSIFICATION; ENVIRONMENTAL FACTOR; GENETIC RISK; GENETIC SUSCEPTIBILITY; HIGH RISK PATIENT; HUMAN; IMMUNE DYSREGULATION; INFLAMMATION; NUCLEAR MAGNETIC RESONANCE IMAGING; PERIODONTAL DISEASE; PORPHYROMONAS GINGIVALIS; POSITRON EMISSION TOMOGRAPHY; PRECLINICAL RHEUMATOID ARTHRITIS; PRIORITY JOURNAL; RHEUMATOID ARTHRITIS; ARTHRITIS, RHEUMATOID; DIAGNOSTIC IMAGING; DISEASE COURSE; EARLY INTERVENTION; ECHOGRAPHY; GENETICS; IMMUNOLOGY; JOINT; PATHOLOGY; PRODROMAL SYMPTOM; RISK ASSESSMENT; RISK FACTOR;

ANTIRHEUMATIC AGENTS; ARTHRITIS, RHEUMATOID; AUTOANTIBODIES; AUTOIMMUNITY; AVIAN PROTEINS; CYTOKINES; DISEASE PROGRESSION; EARLY MEDICAL INTERVENTION; HLA-DRB1 CHAINS; HUMANS; INFLAMMATION; JOINTS; MAGNETIC RESONANCE IMAGING; PRODROMAL SYMPTOMS; RISK ASSESSMENT; RISK FACTORS; ULTRASONOGRAPHY;

EID: 84962129532     PISSN: 23265191     EISSN: 23265205     Source Type: Journal    
DOI: 10.1002/art.39603     Document Type: Article

References (69)

1. 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.
2. Frisell T, Holmqvist M, Kallberg H, Klareskog L, Alfredsson L, Askling J., Familial risks and heritability of rheumatoid arthritis: role of rheumatoid factor/anti-citrullinated protein antibody status, number and type of affected relatives, sex, and age. Arthritis Rheum 2013; 65: 2773-82.
3. Okada Y, Wu D, Trynka G, Raj T, Terao C, Ikari K, et al., Genetics of rheumatoid arthritis contributes to biology and drug discovery. Nature 2014; 506: 376-81.
4. Gregersen PK, Silver J, Winchester RJ., The shared epitope hypothesis: an approach to understanding the molecular genetics of susceptibility to rheumatoid arthritis. Arthritis Rheum 1987; 30: 1205-13.
5. 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.
6. Karlson EW, Deane K., Environmental and gene-environment interactions and risk of rheumatoid arthritis. Rheum Dis Clin North Am 2012; 38: 405-26.
7. Lahiri M, Morgan C, Symmons DP, Bruce IN., Modifiable risk factors for RA: prevention, better than cure? Rheumatology (Oxford) 2012; 51: 499-512.
8. 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.
9. Barra L, Scinocca M, Saunders S, Bhayana R, Rohekar S, Racape M, et al., Anti-citrullinated protein antibodies in unaffected first-degree relatives of rheumatoid arthritis patients. Arthritis Rheum 2013; 65: 1439-47.
10. Arlestig L, Mullazehi M, Kokkonen H, Rocklov J, Ronnelid J, Dahlqvist SR., Antibodies against cyclic citrullinated peptides of IgG, IgA and IgM isotype and rheumatoid factor of IgM and IgA isotype are increased in unaffected members of multicase rheumatoid arthritis families from northern Sweden. Ann Rheum Dis 2012; 71: 825-9.
11. Bos WH, van de Stadt LA, Sohrabian A, Ronnelid J, van Schaardenburg D., Development of anti-citrullinated protein antibody and rheumatoid factor isotypes prior to the onset of rheumatoid arthritis. Arthritis Res Ther 2014; 16: 405.
12. Abou-Raya A, Abou-Raya S, Abu-Elkheir H., Periodontal disease and rheumatoid arthritis: is there a link? Scand J Rheumatol 2005; 34: 408-10.
13. Scher JU, Ubeda C, Equinda M, Khanin R, Buischi Y, Viale A, et al., Periodontal disease and the oral microbiota in new-onset rheumatoid arthritis. Arthritis Rheum 2012; 64: 3083-94.
14. Dissick A, Redman RS, Jones M, Rangan BV, Reimold A, Griffiths GR, et al., Association of periodontitis with rheumatoid arthritis: a pilot study. J Periodontol 2010; 81: 223-30.
15. Albandar JM, Streckfus CF, Adesanya MR, Winn DM., Cigar, pipe, and cigarette smoking as risk factors for periodontal disease and tooth loss. J Periodontol 2000; 71: 1874-81.
16. Marotte H, Farge P, Gaudin P, Alexandre C, Mougin B, Miossec P., The association between periodontal disease and joint destruction in rheumatoid arthritis extends the link between the HLA-DR shared epitope and severity of bone destruction. Ann Rheum Dis 2006; 65: 905-9.
17. McGraw WT, Potempa J, Farley D, Travis J., Purification, characterization, and sequence analysis of a potential virulence factor from Porphyromonas gingivalis, peptidylarginine deiminase. Infect Immun 1999; 67: 3248-56.
18. Wegner N, Wait R, Sroka A, Eick S, Nguyen KA, Lundberg K, et al., Peptidylarginine deiminase from Porphyromonas gingivalis citrullinates human fibrinogen and α-enolase: implications for autoimmunity in rheumatoid arthritis. Arthritis Rheum 2010; 62: 2662-72.
19. Quirke AM, Lugli EB, Wegner N, Hamilton BC, Charles P, Chowdhury M, et al., Heightened immune response to autocitrullinated Porphyromonas gingivalis peptidylarginine deiminase: a potential mechanism for breaching immunologic tolerance in rheumatoid arthritis. Ann Rheum Dis 2014; 73: 263-9.
20. Hendler A, Mulli TK, Hughes FJ, Perrett D, Bombardieri M, Houri-Haddad Y, et al., Involvement of autoimmunity in the pathogenesis of aggressive periodontitis. J Dent Res 2010; 89: 1389-94.
21. Lappin DF, Apatzidou D, Quirke AM, Oliver-Bell J, Butcher JP, Kinane DF, et al., Influence of periodontal disease, Porphyromonas gingivalis and cigarette smoking on systemic anti-citrullinated peptide antibody titres. J Clin Periodontol 2013; 40: 907-15.
22. Mikuls TR, Payne JB, Yu F, Thiele GM, Reynolds RJ, Cannon GW, et al., Periodontitis and Porphyromonas gingivalis in patients with rheumatoid arthritis. Arthritis Rheumatol 2014; 66: 1090-100.
23. Svard A, Kastbom A, Sommarin Y, Skogh T., Salivary IgA antibodies to cyclic citrullinated peptides (CCP) in rheumatoid arthritis. Immunobiology 2013; 218: 232-7.
24. Harvey GP, Fitzsimmons TR, Dhamarpatni AA, Marchant C, Haynes DR, Bartold PM., Expression of peptidylarginine deiminase-2 and -4, citrullinated proteins and anti-citrullinated protein antibodies in human gingiva. J Periodontal Res 2013; 48: 252-61.
25. Makrygiannakis D, Hermansson M, Ulfgren AK, Nicholas AP, Zendman AJ, Eklund A, et al., Smoking increases peptidylarginine deiminase 2 enzyme expression in human lungs and increases citrullination in BAL cells. Ann Rheum Dis 2008; 67: 1488-92.
26. Ytterberg AJ, Joshua V, Reynisdottir G, Tarasova NK, Rutishauser D, Ossipova E, et al., Shared immunological targets in the lungs and joints of patients with rheumatoid arthritis: identification and validation. Ann Rheum Dis 2015; 74: 1772-7.
27. Reynisdottir G, Karimi R, Joshua V, Olsen H, Hensvold AH, Harju A, et al., Structural changes and antibody enrichment in the lungs are early features of anti-citrullinated protein antibody-positive rheumatoid arthritis. Arthritis Rheumatol 2014; 66: 31-9.
28. 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.
29. Willis VC, Demoruelle MK, Derber LA, Chartier-Logan CJ, Parish MC, Pedraza IF, et al., Sputum autoantibodies in patients with established rheumatoid arthritis and subjects at risk of future clinically apparent disease. Arthritis Rheum 2013; 65: 2545-54.
30. Fischer A, Solomon JJ, du Bois RM, Deane KD, Olson AL, Fernandez-Perez ER, et al., Lung disease with anti-CCP antibodies but not rheumatoid arthritis or connective tissue disease. Respir Med 2012; 106: 1040-7.
31. Lederberg J., Infectious history. Science 2000; 288: 287-93.
32. Wu HJ, Ivanov II, Darce J, Hattori K, Shima T, Umesaki Y, et al., Gut-residing segmented filamentous bacteria drive autoimmune arthritis via T helper 17 cells. Immunity 2010; 32: 815-27.
33. Lee YK, Menezes JS, Umesaki Y, Mazmanian SK., Proinflammatory T-cell responses to gut microbiota promote experimental autoimmune encephalomyelitis. Proc Natl Acad Sci U S A 2011; 108 Suppl 1: 4615-22.
34. Round JL, Mazmanian SK., Inducible Foxp3+ regulatory T-cell development by a commensal bacterium of the intestinal microbiota. Proc Natl Acad Sci U S A 2010; 107: 12204-9.
35. Stepankova R, Powrie F, Kofronova O, Kozakova H, Hudcovic T, Hrncir T, et al., Segmented filamentous bacteria in a defined bacterial cocktail induce intestinal inflammation in SCID mice reconstituted with CD45RBhigh CD4+ T cells. Inflamm Bowel Dis 2007; 13: 1202-11.
36. Liu X, Zou Q, Zeng B, Fang Y, Wei H., Analysis of fecal Lactobacillus community structure in patients with early rheumatoid arthritis. Curr Microbiol 2013; 67: 170-6.
37. Scher JU, Sczesnak A, Longman RS, Segata N, Ubeda C, Bielski C, et al., Expansion of intestinal Prevotella copri correlates with enhanced susceptibility to arthritis. Elife 2013; 2: e01202.
38. Vaahtovuo J, Munukka E, Korkeamaki M, Luukkainen R, Toivanen P., Fecal microbiota in early rheumatoid arthritis. J Rheumatol 2008; 35: 1500-5.
39. Zhang X, Zhang D, Jia H, Feng Q, Wang D, Liang D, et al., The oral and gut microbiomes are perturbed in rheumatoid arthritis and partly normalized after treatment. Nat Med 2015; 21: 895-905.
40. Van Steenbergen HW, Huizinga TW, van der Helm-van Mil AH., The preclinical phase of rheumatoid arthritis: what is acknowledged and what needs to be assessed? [review]. Arthritis Rheum 2013; 65: 2219-32.
41. 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.
42. 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.
43. 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.
44. 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.
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. 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.
47. Ramos-Remus C, Castillo-Ortiz JD, Aguilar-Lozano L, Padilla-Ibarra J, Sandoval-Castro C, Vargas-Serafin CO, et al., Autoantibodies in prediction of the development of rheumatoid arthritis among healthy relatives of patients with the disease. Arthritis Rheumatol 2015; 67: 2837-44.
48. 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.
49. 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 2013; 72: 1920-6.
50. Rakieh C, Nam JL, Hunt L, Hensor EM, Das S, Bissell LA, et al., Predicting the development of clinical arthritis in anti-CCP positive individuals with non-specific musculoskeletal symptoms: a prospective observational cohort study. Ann Rheum Dis 2015; 74: 1659-66.
51. Shi J, Knevel R, Suwannalai P, van der Linden MP, Janssen GM, van Veelen PA, et al., Autoantibodies recognizing carbamylated proteins are present in sera of patients with rheumatoid arthritis and predict joint damage. Proc Natl Acad Sci U S A 2011; 108: 17372-7.
52. Gan RW, Trouw LA, Shi J, Toes RE, Huizinga TW, Demoruelle MK, et al., Anti-carbamylated protein antibodies are present prior to rheumatoid arthritis and are associated with its future diagnosis. J Rheumatol 2015; 42: 572-9.
53. Shi J, van de Stadt LA, Levarht EW, Huizinga TW, Toes RE, Trouw LA, et al., Anti-carbamylated protein antibodies are present in arthralgia patients and predict the development of rheumatoid arthritis. Arthritis Rheum 2013; 65: 911-5.
54. 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.
55. Lubbers J, Brink M, van de Stadt LA, Vosslamber S, Wesseling JG, van Schaardenburg D, et al., The type I IFN signature as a biomarker of preclinical rheumatoid arthritis. Ann Rheum Dis 2013; 72: 776-80.
56. Lubbers J, Vosslamber S, van de Stadt LA, van Beers-Tas M, Wesseling JG, von Blomberg BM, et al., B cell signature contributes to the prediction of RA development in patients with arthralgia. Ann Rheum Dis 2015; 74: 1786-8.
57. Stack RJ, van Tuyl LH, Sloots M, van de Stadt LA, Hoogland W, Maat B, et al., Symptom complexes in patients with seropositive arthralgia and in patients newly diagnosed with rheumatoid arthritis: a qualitative exploration of symptom development. Rheumatology (Oxford) 2014; 53: 1646-53.
58. Van Steenbergen HW, van Nies JA, Huizinga TW, Bloem JL, Reijnierse M, van der Helm-van Mil AH., Characterising arthralgia in the preclinical phase of rheumatoid arthritis using MRI. Ann Rheum Dis 2015; 74: 1225-32.
59. Van de Stadt LA, Bos WH, Meursinge Reynders M, 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.
60. De Hair MJ, van de Sande MG, Ramwadhdoebe TH, Hansson M, Landewe R, van der Leij C, et al., Features of the synovium of individuals at risk of developing rheumatoid arthritis: implications for understanding preclinical rheumatoid arthritis. Arthritis Rheumatol 2014; 66: 513-22.
61. Krabben A, Stomp W, van der Heijde DM, van Nies JA, Bloem JL, 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; 72: 1540-4.
62. Gent YY, ter Wee MM, Ahmadi N, van Kuijk C, Voskuyl AE, van der Laken CJ, et al., Three-year clinical outcome following baseline magnetic resonance imaging in anti-citrullinated protein antibody-positive arthralgia patients: an exploratory study. Arthritis Rheumatol 2014; 66: 2909-10.
63. Van Steenbergen HW, van Nies JA, Huizinga TW, Reijnierse M, van der Helm-van Mil AH., Subclinical inflammation on MRI of hand and foot of anticitrullinated peptide antibody-negative arthralgia patients at risk for rheumatoid arthritis. Arthritis Res Ther 2014; 16: R92.
64. 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.
65. 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 2013; 72: 1654-8.
66. Erciyas K, Sezer U, Ustun K, Pehlivan Y, Kisacik B, Senyurt SZ, et al., Effects of periodontal therapy on disease activity and systemic inflammation in rheumatoid arthritis patients. Oral Dis 2013; 19: 394-400.
67. 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.
68. 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.
69. Rangel-Moreno J, Hartson L, Navarro C, Gaxiola M, Selman M, Randall TD., Inducible bronchus-associated lymphoid tissue (iBALT) in patients with pulmonary complications of rheumatoid arthritis. J Clin Invest 2006; 116: 3183-94.