The association between rheumatoid arthritis and periodontitis

Best Practice and Research: Clinical Rheumatology

Volumn 29, Issue 2, 2015, Pages 189-201

  Leech, Michelle T ^a   Bartold, P M ^b  

^a MONASH UNIVERSITY   (Australia)

^b UNIVERSITY OF ADELAIDE   (Australia)

Author keywords

Citrullination; Peptidylarginine deiminase (PAD); Periodontitis (PD); Porphyromonas gingivalis; Rheumatoid arthritis (RA)

Indexed keywords

PROTEIN ARGININE DEIMINASE; HYDROLASE; PROTEIN-ARGININE DEIMINASE;

BACTERIAL INFECTION; DISEASE ASSOCIATION; DOWN REGULATION; DYSBIOSIS; ERYTHROCYTE SEDIMENTATION RATE; GENETIC SUSCEPTIBILITY; GRAM POSITIVE BACTERIUM; HUMAN; IMMUNE RESPONSE; IMMUNITY; IMMUNOREGULATION; INFLAMMATION; NONHUMAN; PATHOGENESIS; PERIODONTAL DISEASE; PERIODONTITIS; PHYSIOLOGICAL PROCESS; PORPHYROMONAS GINGIVALIS; PRIORITY JOURNAL; REVIEW; RHEUMATOID ARTHRITIS; RISK ASSESSMENT; SCIENCE; SMOKING CESSATION; BACTEROIDACEAE INFECTION; ENZYMOLOGY; METABOLISM; MICROBIOLOGY; PATHOGENICITY;

ARTHRITIS, RHEUMATOID; BACTEROIDACEAE INFECTIONS; HUMANS; HYDROLASES; PERIODONTITIS; PORPHYROMONAS GINGIVALIS;

EID: 84941190706     PISSN: 15216942     EISSN: 15321770     Source Type: Journal    
DOI: 10.1016/j.berh.2015.03.001     Document Type: Review

References (77)

1. R. Snyderman, and G.A. MccCarty Analogous mechanisms of tissue destruction in rheumatoid arthritis and periodontal disease. I R.J. Genco, S.E. Mergenhagen, Host-Parasite interaction in periodontal diseases 1982 Washington, DC
2. W.T. McGraw, J. Potempa, D. Farley, and et al. Purification, characterization, and sequence analysis of a potential virulence factor from porphyromonas gingivalis, peptidylarginine deiminase Infect Immun 67 7 1999 3248 3256
3. J.U. Scher, W.A. Bretz, and S.B. Abramson Periodontal disease and subgingival microbiota as contributors for rheumatoid arthritis pathogenesis: modifiable risk factors? Curr Opin Rheumatology 26 4 2014 424 429
4. P.I. Eke, B.A. Dye, L. Wei, and et al. CDC periodontal disease surveillance workgroup: James Beck GDRP. Prevalence of periodontitis in adults in the United States: 2009 and 2010 J Dent Res 91 10 2012 914 920
5. R.P. Darveau, G. Hajishengallis, and M.A. Curtis Porphyromonas gingivalis as a potential community activist for disease J Dent Res 91 9 2012 816 820
6. P.M. Bartold, and T.E. Van Dyke Periodontitis: a host-mediated disruption of microbial homeostasis. Unlearning learned concepts Periodontol 2000 62 1 2013 203 217
7. E. Firatli, A. Kantarci, I. Cebeci, and et al. Association between HLA antigens and early onset periodontitis J Clin Periodontology 23 6 1996 563 566
8. F.B. Mercado, R.I. Marshall, A.C. Klestov, and et al. Relationship between rheumatoid arthritis and periodontitis J Periodontology 72 6 2001 779 787
9. N. Pischon, T. Pischon, J. Kroger, and et al. Association among rheumatoid arthritis, oral hygiene, and periodontitis J Periodontology 79 6 2008 979 986
10. P. de Pablo, T. Dietrich, and T.E. McAlindon Association of periodontal disease and tooth loss with rheumatoid arthritis in the US population J Rheumatology 35 1 2008 70 76
11. T.O. Georgiou, R.I. Marshall, and P.M. Bartold Prevalence of systemic diseases in Brisbane general and periodontal practice patients Aust Dent J 49 4 2004 177 184
12. N.A. Chrysanthakopoulos, and P.A. Chrysanthakopoulos Association between indices of clinically-defined periodontitis and self-reported history of systemic medical conditions J Investigative Clin Dent 2014 July 22 [ePub]
13. T.R. Mikuls, J.B. Payne, F. Yu, and et al. Periodontitis and porphyromonas gingivalis in patients with rheumatoid arthritis Arthritis & Rheumatology 66 5 2014 1090 1100
14. P. Monsarrat, J.N. Vergnes, A. Blaizot, and et al. Oral health status in outpatients with rheumatoid arthritis: the OSARA study Oral Health Dent Manag 13 1 2014 113 119
15. A. Yarwood, T.W. Huizinga, and J. Worthington The genetics of rheumatoid arthritis: risk and protection in different stages of the evolution of RA Rheumatology 2014 Sept 18 [epub]
16. J. Katz, J. Goultschin, R. Benoliel, and et al. Human leukocyte antigen (HLA) DR4. Positive association with rapidly progressing periodontitis J Periodontology 58 9 1987 607 610
17. J.J. Bonfil, F.L. Dillier, P. Mercier, and et al. A "case control" study on the role of HLA DR4 in severe periodontitis and rapidly progressive periodontitis. Identification of types and subtypes using molecular biology (PCR.SSO) J Clin Periodontology 26 2 1999 77 84
18. A.S. Schaefer, A. Jochens, H. Dommisch, and et al. A large candidate-gene association study suggests genetic variants at IRF5 and PRDM1 to be associated with aggressive periodontitis J Clin Periodontology 41 12 2014 1122 1131
19. D. Di Giuseppe, A. Discacciati, N. Orsini, and et al. Cigarette smoking and risk of rheumatoid arthritis: a dose-response meta-analysis Arthritis Res Ther 16 2 2014 R61
20. S.W. Scally, J. Petersen, S.C. Law, and et al. A molecular basis for the association of the HLA-DRB1 locus, citrullination, and rheumatoid arthritis J Exp Med 210 12 2013 2569 2582
21. J.A. Hill, D.A. Bell, W. Brintnell, and et al. Arthritis induced by posttranslationally modified (citrullinated) fibrinogen in DR4-IE transgenic mice J Exp Med 205 4 2008 967 979
22. W. Nesse, J. Westra, J.E. van der Wal, and et al. The periodontium of periodontitis patients contains citrullinated proteins which may play a role in ACPA (anti-citrullinated protein antibody) formation J Clin Periodontology 39 7 2012 599 607
23. G.P. Harvey, T.R. Fitzsimmons, A.A. Dhamarpatni, and et al. Expression of peptidylarginine deiminase-2 and -4, citrullinated proteins and anti-citrullinated protein antibodies in human gingiva J Periodontal Res 48 2 2013 252 261
24. S.S. Socransky, and A.D. Haffajee Dental biofilms: difficult therapeutic targets Periodontol 2000 28 2002 12 55
25. T. Maekawa, J.L. Krauss, T. Abe, and et al. Porphyromonas gingivalis manipulates complement and TLR signaling to uncouple bacterial clearance from inflammation and promote dysbiosis Cell Host Microbe 15 6 2014 768 778
26. A.D. Foey, and S. Crean Macrophage subset sensitivity to endotoxin tolerisation by porphyromonas gingivalis PloS One 8 7 2013 e67955
27. K.S. Kornman, C. Knobelman, and H.Y. Wang Is periodontitis genetic? the answer may be Yes! J Mass Dent Soc 49 3 2000 26 30
28. J.L. Ebersole, D. Cappelli, S.C. Holt, and et al. Gingival crevicular fluid inflammatory mediators and bacteriology of gingivitis in nonhuman primates related to susceptibility to periodontitis Oral Microbiol Immunol 15 1 2000 19 26
29. E. Megson, T. Fitzsimmons, K. Dharmapatni, and et al. C-reactive protein in gingival crevicular fluid may be indicative of systemic inflammation J Clin Periodontology 37 9 2010 797 804
30. N. Priyanka, M. Kumari, N. Kalra, and et al. Crevicular fluid and serum concentrations of progranulin and high sensitivity CRP in chronic periodontitis and type 2 diabetes Dis Markers 35 5 2013 389 394
31. P.J. Perez-Chaparro, C. Goncalves, L.C. Figueiredo, and et al. Newly identified pathogens associated with periodontitis: a systematic review J Dent Res 93 9 2014 846 858
32. E.D. Rosenstein, R.A. Greenwald, L.J. Kushner, and et al. Hypothesis: the humoral immune response to oral bacteria provides a stimulus for the development of rheumatoid arthritis Inflammation 28 6 2004 311 318
33. N. Wegner, R. Wait, A. Sroka, and et al. Peptidylarginine deiminase from porphyromonas gingivalis citrullinates human fibrinogen and alpha-enolase: implications for autoimmunity in rheumatoid arthritis Arthritis Rheumatism 62 9 2010 2662 2672
34. K. Lundberg, C. Bengtsson, N. Kharlamova, and et al. Genetic and environmental determinants for disease risk in subsets of rheumatoid arthritis defined by the anticitrullinated protein/peptide antibody fine specificity profile Ann Rheumatic Dis 72 5 2013 652 658
35. J.U. Scher, C. Ubeda, M. Equinda, and et al. Periodontal disease and the oral microbiota in new-onset rheumatoid arthritis Arthritis Rheumatism 64 10 2012 3083 3094
36. M.D. Cantley, D.R. Haynes, V. Marino, and et al. Pre-existing periodontitis exacerbates experimental arthritis in a mouse model J Clin Periodontology 38 6 2011 532 541
37. K.J. Maresz, A. Hellvard, A. Sroka, and et al. Porphyromonas gingivalis facilitates the development and progression of destructive arthritis through its unique bacterial peptidylarginine deiminase (PAD) PLoS Pathog 9 9 2013 e1003627
38. J.T. Marchesan, E.A. Gerow, R. Schaff, and et al. Porphyromonas gingivalis oral infection exacerbates the development and severity of collagen-induced arthritis Arthritis Res Ther 15 6 2013 R186
39. N. Gully, R. Bright, V. Marino, and et al. Porphyromonas gingivalis peptidylarginine deiminase, a key contributor in the pathogenesis of experimental periodontal disease and experimental arthritis PloS One 9 6 2014 e100838
40. M.F. Konig, A.S. Paracha, M. Moni, and et al. Defining the role of porphyromonas gingivalis peptidylarginine deiminase (PPAD) in rheumatoid arthritis through the study of PPAD biology Ann Rheumatic Dis 10 2014 1399 1405
41. A.M. Quirke, E.B. Lugli, N. Wegner, and et al. Heightened immune response to autocitrullinated porphyromonas gingivalis peptidylarginine deiminase: a potential mechanism for breaching immunologic tolerance in rheumatoid arthritis Ann Rheumatic Dis 73 1 2014 263 269
42. X. Jiang, L.A. Trouw, T.J. van Wesemael, and et al. Anti-CarP antibodies in two large cohorts of patients with rheumatoid arthritis and their relationship to genetic risk factors, cigarette smoking and other autoantibodies Ann Rheumatic Dis 73 10 2014 1761 1768
43. M. Bax, T.W. Huizinga, and R.E. Toes The pathogenic potential of autoreactive antibodies in rheumatoid arthritis Seminars Immunopathol 36 3 2014 313 325
44. J.N. Stoop, B.S. Liu, J. Shi, and et al. Antibodies specific for carbamylated proteins precede the onset of clinical symptoms in mice with collagen induced arthritis PloS One 9 7 2014 e102163
45. C.T. Peterson, V. Sharma, L. Elmen, and et al. Immune homeostasis, dysbiosis and therapeutic modulation of the gut microbiota Clin Exp Immunol 179 3 2014 363 377
46. P.J. Basso, M.T. Fonseca, G. Bonfa, and et al. Association among genetic predisposition, gut microbiota, and host immune response in the etiopathogenesis of inflammatory bowel disease Braz J Med Biological Res = Revista brasileira de pesquisas medicas e biologicas/Sociedade Brasileira de Biofisica [et al] 47 9 2014 727 737
47. A. Couturier-Maillard, T. Secher, A. Rehman, and et al. NOD2-mediated dysbiosis predisposes mice to transmissible colitis and colorectal cancer The Journal of Clinical Investigation 123 2 2013 700 711
48. A. Shusterman, C. Durrant, R. Mott, and et al. Host susceptibility to periodontitis: mapping murine genomic regions Journal of Dental Research 92 5 2013 438 443
49. L. Nibali, D.R. Ready, M. Parkar, and et al. Gene polymorphisms and the prevalence of key periodontal pathogens Journal of Dental Research 86 5 2007 416 420
50. M.M. Jazi, G. Solgi, H.A. Roosta, and et al. HLA-DRB and HLA-DQA/HLA-DQB allele and haplotype frequencies in Iranian patients with aggressive periodontitis Journal of Periodontal Research 48 4 2013 533 539
51. S. Reichert, W. Altermann, J.M. Stein, and et al. Individual composition of human leukocyte antigens and periodontopathogens in the background of periodontitis Journal of Periodontology 84 1 2013 100 109
52. A. Gardette, S. Ottaviani, F. Tubach, and et al. High anti-CCP antibody titres predict good response to rituximab in patients with active rheumatoid arthritis Joint, Bone, Spine: revue du Rhumatisme 81 5 2014 416 420
53. R. Thomas Dendritic cells and the promise of antigen-specific therapy in rheumatoid arthritis Arthritis Research & Therapy 15 1 2013 204
54. C.D. Pack, A.E. Cestra, B. Min, and et al. Neonatal exposure to antigen primes the immune system to develop responses in various lymphoid organs and promotes bystander regulation of diverse T cell specificities Journal of Immunology 167 8 2001 4187 4195
55. N. Svartz The treatment of rheumatic polyarthritis with acid azo compounds Rheumatism 4 1 1948 180 185
56. F.D. Ostrander Vitamins, sulfonamides and antibiotics in periodontal therapy Journal of the American Dental Association 37 3 1948 279 288
57. G. Ash, R. Baker, C. Rajapakse, and et al. Study of sulphamethoxazole in rheumatoid arthritis British Journal of Rheumatology 25 3 1986 285 287
58. R. Nakao, S. Takigawa, N. Sugano, and et al. Impact of minocycline ointment for periodontal treatment of oral bacteria Japanese Journal of Infectious Diseases 64 2 2011 156 160
59. P.M. Bartold, A.H. du Bois, S. Gannon, and et al. Antibacterial and immunomodulatory properties of azithromycin treatment implications for periodontitis Inflammopharmacology 21 4 2013 321 338
60. M. Ogrendik Effects of clarithromycin in patients with active rheumatoid arthritis Current Medical Research and Opinion 23 3 2007 515 522
61. G. Saviola, L. Abdi-Ali, L. Campostrini, and et al. Clarithromycin in rheumatoid arthritis: the addition to methotrexate and low-dose methylprednisolone induces a significant additive value-a 24-month single-blind pilot study Rheumatology International 33 11 2013 2833 2838
62. M. Ogrendik, and N. Karagoz Treatment of rheumatoid arthritis with roxithromycin: a randomized trial Postgraduate Medicine 123 5 2011 220 227
63. M. Ogrendik Levofloxacin treatment in patients with rheumatoid arthritis receiving methotrexate Southern Medical Journal 100 2 2007 135 139
64. A.R. Amin, M.G. Attur, G.D. Thakker, and et al. A novel mechanism of action of tetracyclines: effects on nitric oxide synthases Proceedings of the National Academy of Sciences of the U. S. A 93 24 1996 14014 14019
65. C.J. Doyle, T.R. Fitzsimmons, C. Marchant, and et al. Azithromycin suppresses P. gingivalis LPS-induced pro-inflammatory cytokine and chemokine production by human gingival fibroblasts in vitro Clinical Oral Investigations 19 2 2014 221 227
66. A. Suzuki, R. Yamada, and K. Yamamoto Citrullination by peptidylarginine deiminase in rheumatoid arthritis Annals of the N. Y Academy of Sciences 1108 2007 323 339
67. C. Foulquier, M. Sebbag, C. Clavel, and et al. Peptidyl arginine deiminase type 2 (PAD-2) and PAD-4 but not PAD-1, PAD-3, and PAD-6 are expressed in rheumatoid arthritis synovium in close association with tissue inflammation Arthritis and rheumatism 56 11 2007 3541 3553
68. B. Knuckley, Y. Luo, and P.R. Thompson Profiling protein Arginine Deiminase 4 (PAD4): a novel screen to identify PAD4 inhibitors Bioorganic & Medicinal Chemistry 16 2 2008 739 745
69. V.C. Willis, A.M. Gizinski, N.K. Banda, and et al. N-alpha-benzoyl-N5-(2-chloro-1-iminoethyl)-L-ornithine amide, a protein arginine deiminase inhibitor, reduces the severity of murine collagen-induced arthritis Journal of Immunology 186 7 2011 4396 4404
70. S.K. Bhattacharya, M.B. Bhat, and H. Takahara Modulation of peptidyl arginine deiminase 2 and implication for neurodegeneration Current Eye Research 31 12 2006 1063 1071
71. S. Lange, E. Rocha-Ferreira, L. Thei, and et al. Peptidylarginine deiminases: novel drug targets for prevention of neuronal damage following hypoxic ischemic insult (HI) in neonates Journal of Neurochemistry 130 4 2014 555 562
72. C.J. Dreyton, J.E. Jones, B.A. Knuckley, and et al. Optimization and characterization of a pan protein arginine deiminase (PAD) inhibitor 2010 Probe Reports from the NIH Molecular Libraries Program Bethesda (MD)
73. K.L. Bicker, L. Anguish, A.A. Chumanevich, and et al. D-amino acid based protein arginine deiminase inhibitors: synthesis, pharmacokinetics, and in cellulo efficacy ACS Medicinal Chemistry Letters 3 12 2012 1081 1085
74. C.I. Daien, and J. Morel Predictive factors of response to biological disease modifying antirheumatic drugs: towards personalized medicine Mediators of Inflammation 2014 2014 386148
75. L. Chambrone, P.M. Preshaw, E.F. Rosa, and et al. Effects of smoking cessation on the outcomes of non-surgical periodontal therapy: a systematic review and individual patient data meta-analysis Journal of Clinical Periodontology 40 6 2013 607 615
76. J.A. Sparks, M.D. Iversen, R. Miller Kroouze, and et al. Personalized risk estimator for rheumatoid Arthritis (PRE-RA) family Study: rationale and design for a randomized controlled trial evaluating rheumatoid arthritis risk education to first-degree relatives Contemporary Clinical Trials 39 1 2014 145 157
77. L.A. van de Stadt, M.H. de Koning, R.J. van de Stadt, and et al. Development of the anti-citrullinated protein antibody repertoire prior to the onset of rheumatoid arthritis Arthritis and Rheumatism 63 11 2011 3226 3233