2,079
Views
66
CrossRef citations to date
0
Altmetric
Review Articles

Rheumatoid arthritis and periodontitis – inflammatory and infectious connections. Review of the literature

Article: 11829 | Received 06 Nov 2011, Accepted 23 Jan 2012, Published online: 13 Feb 2012

References

  • Sacks JJ, Luo YH, Helmick CG. Prevalence of specific types of arthritis and other rheumatic conditions in the ambulatory health care system in the United States, 2001–2005. Arthritis Care Res. 2010; 62: 460–4.
  • Myasoedova E, Crowson CS, Kremers HM, Therneau TM, Gabriel SE. Is the incidence of rheumatoid arthritis rising? results from Olmsted County, Minnesota, 1955–2007. Arthritis Rheum. 2010; 62: 1576–82.
  • Silman AJ, Hochberg MC. Epidemiology of the rheumatic diseases. , second ed. New York: Oxford University Press. 2001.
  • Available from: http://www.rheumatology.org/practice/clinical/classification/ra/ra_2010.asp [ cited 14 October 2011]
  • Page RC, Eke PI. Case definitions for use in population-based surveillance of periodontitis. J Periodontol. 2007; 78: 1387–99.
  • Armitage GC. Manual periodontal probing in supportive periodontal treatment 2000. Periodontol. 1996; 12: 33–9.
  • Anonymous. An Evaluation of the effect of dental focal infection on health. JADA. 1952; 42: 609–97.
  • Desvarieux M, Demmer RT, Rundek T, Boden-Albala B, Jacobs DR Jr, Sacco RL, et al.. Periodontal microbiota and carotid intima-media thickness: the Oral Infections and Vascular Disease Epidemiology Study (INVEST). Circulation. 2005; 111: 576–82.
  • Hayashi C, Gudino CV, Gibson FC III, Genco CA. Review: pathogen-induced inflammation at sites distant from oral infection: bacterial persistence and induction of cell-specific innate immune inflammatory pathways. Mol Oral Microbiol. 2010; 25: 305–16.
  • Taylor BA, Tofler GH, Carey HM, Morel-Kopp MC, Philcox S, Carter TR, et al.. Full-mouth tooth extraction lowers systemic inflammatory and thrombotic markers of cardiovascular risk. J Dent Res. 2006; 85: 74–8.
  • Tonetti MS, D'Aiuto F, Nibali L, Donald A, Storry C, Parkar M, et al.. Treatment of periodontitis and endothelial function. N Engl J Med. 2007; 356: 911–20.
  • Lindhe J, Okamoto H, Yoneyama T, Haffajee A, Socransky SS. Longitudinal changes in periodontal disease in untreated subjects. J Clin Periodontol. 1989; 16: 662–70.
  • Persson GR, DeRouen TA, Page RC. Relationship between gingival crevicular fluid levels of aspartate aminotransferase and active tissue destruction in treated chronic periodontitis patients. J Periodontal Res. 1990; 25: 81–7.
  • Papapanou PN, Behle JH, Kebschull M, Celenti R, Wolf DL, Handfield M, et al.. Subgingival bacterial colonization profiles correlate with gingival tissue gene expression. BMC Microbiol. 2009; 9: 221.
  • Paster BJ, Olsen I, Aas JA, Dewhirst FE. The breadth of bacterial diversity in the human periodontal pocket and other oral sites 2000. Periodontol. 2006; 42: 80–7.
  • Preza D, Olsen I, Willumsen T, Grinde B, Paster BJ. Diversity and site-specificity of the oral microflora in the elderly. Eur J Clin Microbiol Infect Dis. 2009; 28: 33–40.
  • Fredericks DN, Relman DA. Sequence-based identification of microbial pathogens: a reconsideration of Koch's postulates. Clin Microbiol Rev. 1996; 9: 18–33.
  • Holt SC, Ebersole J, Felton J, Brunsvold M, Kornman KS. Implantation of Bacteroides gingivalis in nonhuman primates initiates progression of periodontitis. Science. 1988; 239: 55–7.
  • Persson GR, Engel D, Whitney C, Darveau R, Weinberg A, Brunsvold M, et al.. Immunization against Porphyromonas gingivalis inhibits progression of experimental periodontitis in nonhuman primates. Infect Immun. 1994; 62: 1026–31.
  • Moritz AJ, Cappelli D, Lantz MS, Holt SC, Ebersole JL. Immunization with Porphyromonas gingivalis cysteine protease: effects on experimental gingivitis and ligature-induced periodontitis in Macaca fascicularis. J Periodontol. 1998; 69: 686–97.
  • Page RC, Lantz MS, Darveau R, Jeffcoat M, Mancl L, Houston L, et al.. Immunization of Macaca fascicularis against experimental periodontitis using a vaccine containing cysteine proteases purified from Porphyromonas gingivalis. Oral Microbiol Immunol. 2007; 22: 162–8.
  • Strauss J, Kaplan GG, Beck PL, Rioux K, Panaccione R, Devinney R, et al.. Invasive potential of gut mucosa-derived Fusobacterium nucleatum positively correlates with IBD status of the host. Inflamm Bowel Dis. 2011; 17: 1971–8.
  • Brook I. Role of anaerobic bacteria in infections following tracheostomy, intubation, or the use of ventilatory tubes in children. Ann Otol Rhinol Laryngol. 2004; 113: 830–4.
  • Nikolaitchouk N, Andersch B, Falsen E, Strömbeck L, Mattsby-Baltzer I. The lower genital tract microbiota in relation to cytokine-, SLPI- and endotoxin levels: application of checkerboard DNA-DNA hybridization (CDH). APMIS. 2008; 116: 263–77.
  • Persson R, Hitti J, Verhelst R, Vaneechoutte M, Persson R, Hirschi R, et al.. The vaginal microflora in relation to gingivitis. BMC Infect Dis. 2009; 9: 6.
  • Cotsapas C, Voight BF, Rossin E, Lage K, Neale BM, Wallace C, et al.. FOCiS Network of Consortia. Pervasive sharing of genetic effects in autoimmune disease. PLoS Genet. 2011; 7: e1002254.
  • Schäfer AS, Jepsen S, Loos BG. Periodontal genetics: a decade of genetic association studies mandates better study designs. J Clin Periodontol. 2011; 38: 103–7.
  • Nakaoka H, Cui T, Tajima A, Oka A, Mitsunaga S, Kashiwase K, et al.. A systems genetics approach provides a bridge from discovered genetic variants to biological pathways in rheumatoid arthritis. PLoS One. 2011; 6: e25389.
  • Rodríguez-Rodríguez L, Lamas JR, Varadé J, Tornero-Esteban P, Abasolo L, de la Concha EG, et al.. Combined influence of genetic and environmental factors in age of rheumatoid arthritis onset. Rheumatol Int. 2011. 10.3402/jom.v4i0.11829.
  • Costenbader KH, Prescott J, Zee RY, De Vivo I. Immunosenescence and rheumatoid arthritis: does telomere shortening predict impending disease?. Autoimmun Rev. 2011; 10: 569–73.
  • Ospelt C, Reedquist KA, Gay S, Tak PP. Inflammatory memories: is epigenetics the missing link to persistent stromal cell activation in rheumatoid arthritis?. Autoimmun Rev. 2011; 10: 519–24.
  • Gomez RS, Dutra WO, Moreira PR. Epigenetics and periodontal disease: future perspectives. Inflamm Res. 2009; 58: 625–9.
  • Grabiec AM, Reedquist KA. Histone deacetylases in RA: epigenetics and epiphenomena. Arthritis Res Ther. 2010; 12: 142.
  • McCall CE, Yoza B, Liu T, El Gazzar M. Gene-specific epigenetic regulation in serious infections with systemic inflammation. J Innate Immun. 2010; 2: 395–405.
  • Rantapää-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.
  • Rosenstein ED, Greenwald RA, Kushner LJ, Weissmann G. Hypothesis: the humoral immune response to oral bacteria provides a stimulus for the development of rheumatoid arthritis. Inflammation. 2004; 28: 311–8.
  • 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.
  • Lundberg K, Wegner N, Yucel-Lindberg T, Venables PJ. Periodontitis in RA—the citrullinated enolase connection. Nat Rev Rheumatol. 2010; 6: 727–30.
  • Kinloch A, Lundberg K, Wait R, Wegner N, Lim NH, Zendman AJ, et al.. Synovial fluid is a site of citrullination of autoantigens in inflammatory arthritis. Arthritis Rheum. 2008; 58: 2287–95.
  • Lundberg K, Kinloch A, Fisher BA, Wegner N, Wait R, Charles P, et al.. Antibodies to citrullinated alpha-enolase peptide 1 are specific for rheumatoid arthritis and cross-react with bacterial enolase. Arthritis Rheum. 2008; 58: 3009–19.
  • Nigrovic PA, Lee DM. Synovial mast cells: role in acute and chronic arthritis. Immunol Rev. 2007; 217: 19–37.
  • Vandooren B, Cantaert T, Noordenbos T, Tak PP, Baeten D. The abundant synovial expression of the RANK/RANKL/Osteoprotegerin system in peripheral spondylarthritis is partially disconnected from inflammation. Arthritis Rheum. 2008; 58: 718–29.
  • Wang Q, Ma Y, Liu D, Zhang L, Wei W. The roles of B cells and their interactions with fibroblast-like synoviocytes in the pathogenesis of rheumatoid arthritis. Int Arch Allergy Immunol. 2011; 155: 205–11.
  • Choy E. New biologics for rheumatoid arthritis. J R Coll Physicians Edinb. 2011; 41: 234–7.
  • Astry B, Harberts E, Moudgil KD. A cytokine-centric view of the pathogenesis and treatment of autoimmune arthritis. J Interferon Cytokine Res. 2011; 31: 927–40.
  • Romas E, Gillespie MT, Martin TJ. Involvement of receptor activator of NFkappaB ligand and tumor necrosis factor-alpha in bone destruction in rheumatoid arthritis. Bone. 2002; 30: 340–6.
  • Hernández M, Dutzan N, García-Sesnich J, Abusleme L, Dezerega A, Silva N, et al.. Host-pathogen interactions in progressive chronic periodontitis. J Dent Res. 2011; 90: 1164–70.
  • Orita S, Koshi T, Mitsuka T, Miyagi M, Inoue G, Arai G, et al.. Associations between proinflammatory cytokines in the synovial fluid and radiographic grading and pain-related scores in 47 consecutive patients with osteoarthritis of the knee. BMC Musculoskelet Disord. 2011; 12: 144.
  • Preshaw PM, Taylor JJ. How has research into cytokine interactions and their role in driving immune responses impacted our understanding of periodontitis?. J Clin Periodontol. 2011; 38: 60–84.
  • Fagundes JA, Monoo LD, Euzébio Alves VT, Pannuti CM, Cortelli SC, Cortelli JR, et al.. Porphyromonas gingivalis is associated with protease-activated receptor-2 up-regulation in chronic periodontitis. J Periodontol. 2011; 82: 1596–601.
  • Belibasakis GN, Bostanci N, Reddi D. Regulation of protease-activated receptor-2 expression in gingival fibroblasts and Jurkat T cells by Porphyromonas gingivalis. Cell Biol Int. 2010; 34: 287–92.
  • Mercado RB, Marshall RI, Klestov AC, Bartold PM. Relationship between rheumatoid arthritis and periodontitis. J Periodontol. 2001; 72: 779–87.
  • Arnett FC, Edworthy SM, Bloch DA, McShane DJ, Fries JF, Cooper NS, et al.. The American Rheumatism Association 1987 revised criteria for the classification of rheumatoid arthritis. Arthritis Rheum. 1988; 31: 315–24.
  • Moen K, Brun JG, Valen M, Skartveit L, Eribe EK, Olsen I, et al.. Synovial inflammation in active rheumatoid arthritis and psoriatic arthritis facilitates trapping of a variety of oral bacterial DNAs. Clin Exp Rheumatol. 2006; 24: 656–63.
  • Kobayashi T, Ito S, Kuroda T, Yamamoto K, Sugita N, Narita I, et al.. The interleukin-1 and Fcgamma receptor gene polymorphisms in Japanese patients with rheumatoid arthritis and periodontitis. J Periodontol. 2007; 78: 2311–8.
  • Leksell E, Ernberg M, Magnusson B, Hedenberg-Magnusson B. Intraoral condition in children with juvenile idiopathic arthritis compared to controls. Int J Paediatr Dent. 2008; 18: 423–33.
  • de Pablo P, Dietrich T, McAlindon TE. Association of periodontal disease and tooth loss with rheumatoid arthritis in the US population. J Rheumatol. 2008; 35: 70–6.
  • Nilsson M, Kopp S. Gingivitis and periodontitis are related to repeated high levels of circulating tumor necrosis factor-alpha in patients with rheumatoid arthritis. J Periodontol. 2008; 79: 1689–96.
  • Pischon N, Pischon T, Kröger J, Gülmez E, Kleber BM, Bernimoulin JP, et al.. Association among rheumatoid arthritis, oral hygiene, and periodontitis. J Periodontol. 2008; 79: 979–86.
  • Prevoo ML, van't Hof MA, Kuper HH, van Leeuwen MA, van de Putte LB, van Riel PL. Modified disease activity scores that include twenty-eight-joint counts. Development and validation in a prospective longitudinal study of patients with rheumatoid arthritis. Arthritis Rheum. 1995; 38: 44–8.
  • Biyikoğlu B, Buduneli N, Kardeşler L, Aksu K, Pitkala M, Sorsa T. Gingival crevicular fluid MMP-8 and -13 and TIMP-1 levels in patients with rheumatoid arthritis and inflammatory periodontal disease. J Periodontol. 2009; 80: 1307–14.
  • Martinez-Martinez RE, Abud-Mendoza C, Patiño-Marin N, Rizo-Rodríguez JC, Little JW, Loyola-Rodríguez JP. Detection of periodontal bacterial DNA in serum and synovial fluid in refractory rheumatoid arthritis patients. J Clin Periodontol. 2009; 36: 1004–10.
  • 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.
  • Trombone AP, Claudino M, Colavite P, de Assis GF, Avila-Campos MJ, Silva JS, et al.. Periodontitis and arthritis interaction in mice involves a shared hyper-inflammatory genotype and functional immunological interferences. Genes Immun. 2010; 11: 479–89.
  • Mirrielees J, Crofford LJ, Lin Y, Kryscio RJ, Dawson DR III, Ebersole JL, et al.. Rheumatoid arthritis and salivary biomarkers of periodontal disease. J Clin Periodontol. 2010; 37: 1068–74.
  • Okada M, Kobayashi T, Ito S, Yokoyama T, Komatsu Y, Abe A, et al.. Antibody responses to periodontopathic bacteria in relation to rheumatoid arthritis in Japanese adults. J Periodontol. 2011; 82: 1433–41.
  • Ziebolz D, Pabel SO, Lange K, Krohn-Grimberghe B, Hornecker E, Mausberg RF. Clinical periodontal and microbiologic parameters in patients with rheumatoid arthritis. J Periodontol. 2011; 82: 1424–2.
  • Börgeson E, Lönn J, Bergström I, Brodin VP, Ramström S, Nayeri F, et al.. Lipoxin A4 inhibits Porphyromonas gingivalis-induced aggregation and reactive oxygen species production by modulating neutrophil-platelet interaction and CD11b expression. Infect Immun. 2011; 79: 1489–97.
  • Pouliot M, Clish CB, Petasis NA, Van Dyke TE, Serhan CN. Lipoxin A4 analogues inhibit leukocyte recruitment to Porphyromonas gingivalis: a role for cyclooxygenase-2 and lipoxins in periodontal disease. Biochemistry. 2000; 39: 4761–8.
  • Elkhouli AM. The efficacy of host response modulation therapy (omega-3 plus low-dose aspirin) as an adjunctive treatment of chronic periodontitis (clinical and biochemical study). J Periodontal Res. 2011; 46: 261–8.
  • Emingil G, Gürkan A, Atilla G, Kantarci A. Subantimicrobial-dose doxycycline and cytokine-chemokine levels in gingival crevicular fluid. J Periodontol. 2011; 82: 452–61.
  • Al-Katma MK, Bissada NF, Bordeaux JM, Sue J, Askari AD. Control of periodontal infection reduces the severity of active rheumatoid arthritis. J Clin Rheumatol. 2007; 13: 134–7.
  • Pers JO, Saraux A, Pierre R, Youinou P. Anti-TNF-alpha immunotherapy is associated with increased gingival inflammation without clinical attachment loss in subjects with rheumatoid arthritis. J Periodontol. 2008; 79: 1645–51.
  • Miranda LA, Islabão AG, Fischer RG, Figueredo CM, Oppermann RV, Gustafsson A. Decreased interleukin-1beta and elastase in the gingival crevicular fluid of individuals undergoing anti-inflammatory treatment for rheumatoid arthritis. J Periodontol. 2007; 78: 1612–9.
  • Mayer Y, Balbir-Gurman A, Machtei EE. Anti-tumor necrosis factor-alpha therapy and periodontal parameters in patients with rheumatoid arthritis. J Periodontol. 2009; 80: 1414–20.
  • Ribeiro J, Leão A, Novaes AB. Periodontal infection as a possible severity factor for rheumatoid arthritis. J Clin Periodontol. 2005; 32: 412–6.
  • Pinho Mde N, Oliveira RD, Novaes AB Jr, Voltarelli JC. Relationship between periodontitis and rheumatoid arthritis and the effect of non-surgical periodontal treatment. Braz Dent J. 2009; 20: 355–64.
  • Ortiz P, Bissada NF, Palomo L, Han YW, Al-Zahrani MS, Panneerselvam A, et al.. Periodontal therapy reduces the severity of active rheumatoid arthritis in patients treated with or without tumor necrosis factor inhibitors. J Periodontol. 2009; 80: 535–40.
  • Queiroz-Junior CM, Madeira MF, Coelho FM, Costa VV, Bessoni RL, Sousa LF, et al.. Experimental arthritis triggers periodontal disease in mice: involvement of TNF-{alpha} and the oral microbiota. J Immunol. 2011; 187: 3821–30.
  • Strangfeld A, Eveslage M, Schneider M, Bergerhausen HJ, Klopsch T, Zink A, Listing J. Treatment benefit or survival of the fittest: what drives the time-dependent decrease in serious infection rates under TNF inhibition and what does this imply for the individual patient?. Ann Rheum Dis. 2011; 70: 1914–20.
  • Komano Y, Tanaka M, Nanki T, Koike R, Sakai R, Kameda H, et al.. REAL Study Group. Incidence and risk factors for serious infection in patients with rheumatoid arthritis treated with tumor necrosis factor inhibitors: a report from the Registry of Japanese Rheumatoid Arthritis Patients for Longterm Safety. J Rheumatol. 2011; 38: 1258–64.
  • Hassan SZ, Gheita TA, Kenawy SA, Fahim AT, El-Sorougy IM, Abdou MS. Oxidative stress in systemic lupus erythematosus and rheumatoid arthritis patients: relationship to disease manifestations and activity. Int J Rheum Dis. 2011; 14: 325–31.
  • Park MK, Park JS, Cho ML, Oh HJ, Heo YJ, Woo YJ, et al.. Grape seed proanthocyanidin extract (GSPE) differentially regulates Foxp3(+) regulatory and IL-17(+) pathogenic T cell in autoimmune arthritis. Immunol Lett. 2011; 135: 50–8.
  • Calder PC, Albers R, Antoine JM, Blum S, Bourdet-Sicard R, Ferns GA, et al.. Inflammatory disease processes and interactions with nutrition. Br J Nutr. 2009; 101: S1–45.
  • McKay JA, Mathers JC. Diet induced epigenetic changes and their implications for health. Acta Physiol (Oxf). 2011; 202: 103–18.
  • Hänninen, Kaartinen K, Rauma AL, Nenonen M, Törrönen R, Häkkinen AS, et al.. Antioxidants in vegan diet and rheumatic disorders. Toxicology. 2000; 155: 45–53.
  • van Vugt RM, Rijken PJ, Rietveld AG, van Vugt AC, Dijkmans BA. Antioxidant intervention in rheumatoid arthritis: results of an open pilot study. Clin Rheumatol. 2008; 27: 771–5.
  • Bahadori B, Uitz E, Thonhofer R, Trummer M, Pestemer-Lach I, McCarty M, et al.. omega-3 Fatty acids infusions as adjuvant therapy in rheumatoid arthritis. J Parenter Enteral Nutr. 2010; 34: 151–5.
  • Bonifait L, Grenier D. Cranberry polyphenols: potential benefits for dental caries and periodontal disease. J Can Dent Assoc. 2010; 76: a130.
  • Oguz KK, Kurne A, Aksu AO, Karabulut E, Serdaroglu A, Teber S, et al.. Assessment of citrullinated myelin by 1H-MR spectroscopy in early-onset multiple sclerosis. Am J Neuroradiol. 2009; 30: 716–21.
  • Wegner N, Lundberg K, Kinloch A, Fisher B, Malmström V, Feldmann M, et al.. Autoimmunity to specific citrullinated proteins gives the first clues to the etiology of rheumatoid arthritis. Immunol Rev. 2010; 233: 34–54.
  • Sweier DG, Shelburne PS, Giannobile WV, Kinney JS, Lopatin DE, Shelburne CE. Immunoglobulin G (IgG) class, but Not IgA or IgM, antibodies to peptides of the Porphyromonas gingivalis chaperone HtpG predict health in subjects with periodontitis by a fluorescence enzyme-linked immunosorbent assay. Clin Vaccine Immunol. 2009; 16: 1766–73.
  • Choi J, Lee SY, Kim K, Choi BK. Identification of immunoreactive epitopes of the Porphyromonas gingivalis heat shock protein in periodontitis and atherosclerosis. J Periodontal Res. 2011; 46: 240–5.
  • Seymour GJ, Ford PJ, Cullinan MP, Leishman S, Yamazaki K. Relationship between periodontal infections and systemic disease. Clin Microbiol Infect. 2007; 13: 3–10.
  • Wu CT, Ou LS, Yeh KW, Lee WI, Huang JL. Serum heat shock protein 60 can predict remission of flare-up in juvenile idiopathic arthritis. Clin Rheumatol. 2011; 30: 959–65.
  • Bodnár N, Szekanecz Z, Prohászka Z, Kemény-Beke A, Némethné-Gyurcsik Z, Gulyás K, et al.. Anti-mutated citrullinated vimentin (anti-MCV) and anti-65kDa heat shock protein (anti-hsp65): New biomarkers in ankylosing spondylitis. Joint Bone Spine. 2012; 79: 63–6.