Skip to main content
Erschienen in: Clinical Oral Investigations 1/2017

25.08.2016 | Review

Serum antibody levels against Porphyromonas gingivalis in patients with and without rheumatoid arthritis – a systematic review and meta-analysis

verfasst von: Philip Bender, Walter B. Bürgin, Anton Sculean, Sigrun Eick

Erschienen in: Clinical Oral Investigations | Ausgabe 1/2017

Einloggen, um Zugang zu erhalten

Abstract

Objectives

Since the peptidyl arginine deiminase of Porphyromonas gingivalis is able to citrullinate peptides and proteins, various studies have suggested the species as a possible link between periodontal disease (PD) and rheumatoid arthritis (RA). This systematic review including meta-analysis was aimed to evaluate whether differences in terms of antibody titers against P. gingivalis exist between RA patients and systemically healthy individuals with and without PD.

Materials and methods

The following focused question was addressed: Are the antibody titers against P. gingivalis of RA patients different from systemically healthy individuals with and without PD? A systematic data search was conducted in MEDLINE and EMBASE. The collected data underwent a meta-analysis to detect statistically significant differences in terms of antibody levels between the groups.

Results

From 114 articles found by the search 13 articles met the inclusion criteria and provided data suitable for meta-analysis. After analyzing various levels of confinement the meta-analysis revealed a statistically significant higher antibody titer against P. gingivalis in patients suffering from RA in comparison with systemically and periodontally healthy controls (p < 0.01) and systemically healthy patients with PD (p < 0.01).

Conclusion

The present findings indicate that RA is often accompanied by the presence of an immune response against P. gingivalis.

Clinical relevance

The significantly higher antibody response to P. gingivalis in comparison to systemically healthy individuals supports the link between PD and RA by P. gingivalis. Screening of the regularly taken blood samples of RA patients for P. gingivalis antibodies may help to sensitize rheumatologists and RA patients for improving periodontal health.
Literatur
1.
Zurück zum Zitat de Pablo P, Dietrich T, McAlindon TE (2008) Association of periodontal disease and tooth loss with rheumatoid arthritis in the US population. J Rheumatol 35:70–76PubMed de Pablo P, Dietrich T, McAlindon TE (2008) Association of periodontal disease and tooth loss with rheumatoid arthritis in the US population. J Rheumatol 35:70–76PubMed
2.
Zurück zum Zitat Dissick A, Redman RS, Jones M, Rangan BV, Reimold A, Griffiths GR, Mikuls TR, Amdur RL, Richards JS, Kerr GS (2010) Association of periodontitis with rheumatoid arthritis: a pilot study. J Periodontol 81:223–230. doi:10.1902/jop.2009.090309 CrossRefPubMed Dissick A, Redman RS, Jones M, Rangan BV, Reimold A, Griffiths GR, Mikuls TR, Amdur RL, Richards JS, Kerr GS (2010) Association of periodontitis with rheumatoid arthritis: a pilot study. J Periodontol 81:223–230. doi:10.​1902/​jop.​2009.​090309 CrossRefPubMed
4.
Zurück zum Zitat Snyderman, R MG (1982) Analogous mechanisms of tissue destruction in rheumatoid arthritis and periodontal disease. Book title., Snyderman, R MG (1982) Analogous mechanisms of tissue destruction in rheumatoid arthritis and periodontal disease. Book title.,
5.
Zurück zum Zitat Jiang P, Li H, Li X (2015) Diabetes mellitus risk factors in rheumatoid arthritis: a systematic review and meta-analysis. Clin Exp Rheumatol 33:115–121PubMed Jiang P, Li H, Li X (2015) Diabetes mellitus risk factors in rheumatoid arthritis: a systematic review and meta-analysis. Clin Exp Rheumatol 33:115–121PubMed
10.
Zurück zum Zitat Biyikoglu B, Buduneli N, Aksu K, Nalbantsoy A, Lappin DF, Evrenosoglu E, Kinane DF (2013) Periodontal therapy in chronic periodontitis lowers gingival crevicular fluid interleukin-1beta and DAS28 in rheumatoid arthritis patients. Rheumatol Int. doi:10.1007/s00296-013-2781-5 PubMed Biyikoglu B, Buduneli N, Aksu K, Nalbantsoy A, Lappin DF, Evrenosoglu E, Kinane DF (2013) Periodontal therapy in chronic periodontitis lowers gingival crevicular fluid interleukin-1beta and DAS28 in rheumatoid arthritis patients. Rheumatol Int. doi:10.​1007/​s00296-013-2781-5 PubMed
11.
Zurück zum Zitat Erciyas K, Sezer U, Ustun K, Pehlivan Y, Kisacik B, Senyurt SZ, Tarakcioglu M, Onat AM (2013) Effects of periodontal therapy on disease activity and systemic inflammation in rheumatoid arthritis patients. Oral Dis 19:394–400. doi:10.1111/odi.12017 CrossRefPubMed Erciyas K, Sezer U, Ustun K, Pehlivan Y, Kisacik B, Senyurt SZ, Tarakcioglu M, Onat AM (2013) Effects of periodontal therapy on disease activity and systemic inflammation in rheumatoid arthritis patients. Oral Dis 19:394–400. doi:10.​1111/​odi.​12017 CrossRefPubMed
12.
Zurück zum Zitat Ustun K, Erciyas K, Kisacik B, Sezer U, Pehlivan Y, Oztuzcu S, Gundogar H, Onat AM (2013) Host modulation in rheumatoid arthritis patients with TNF blockers significantly decreases biochemical parameters in periodontitis. Inflammation. doi:10.1007/s10753-013-9652-9 Ustun K, Erciyas K, Kisacik B, Sezer U, Pehlivan Y, Oztuzcu S, Gundogar H, Onat AM (2013) Host modulation in rheumatoid arthritis patients with TNF blockers significantly decreases biochemical parameters in periodontitis. Inflammation. doi:10.​1007/​s10753-013-9652-9
13.
Zurück zum Zitat Mayer Y, Elimelech R, Balbir-Gurman A, Braun-Moscovici Y, Machtei EE (2013) Periodontal condition of patients with autoimmune diseases and the effect of anti-tumor necrosis factor-alpha therapy. J Periodontol 84:136–142. doi:10.1902/jop.2012.120009 CrossRefPubMed Mayer Y, Elimelech R, Balbir-Gurman A, Braun-Moscovici Y, Machtei EE (2013) Periodontal condition of patients with autoimmune diseases and the effect of anti-tumor necrosis factor-alpha therapy. J Periodontol 84:136–142. doi:10.​1902/​jop.​2012.​120009 CrossRefPubMed
14.
Zurück zum Zitat Savioli C, Ribeiro AC, Fabri GM, Calich AL, Carvalho J, Silva CA, Viana VS, Bonfa E, Siqueira JT (2012) Persistent periodontal disease hampers anti-tumor necrosis factor treatment response in rheumatoid arthritis. J Clin Rheumatol 18:180–184. doi:10.1097/RHU.0b013e31825828be PubMed Savioli C, Ribeiro AC, Fabri GM, Calich AL, Carvalho J, Silva CA, Viana VS, Bonfa E, Siqueira JT (2012) Persistent periodontal disease hampers anti-tumor necrosis factor treatment response in rheumatoid arthritis. J Clin Rheumatol 18:180–184. doi:10.​1097/​RHU.​0b013e31825828be​ PubMed
16.
17.
Zurück zum Zitat Rosenstein ED, Greenwald RA, Kushner LJ, Weissmann G (2004) Hypothesis: the humoral immune response to oral bacteria provides a stimulus for the development of rheumatoid arthritis. Inflammation 28:311–318. doi:10.1007/s10753-004-6641-z CrossRefPubMed Rosenstein ED, Greenwald RA, Kushner LJ, Weissmann G (2004) Hypothesis: the humoral immune response to oral bacteria provides a stimulus for the development of rheumatoid arthritis. Inflammation 28:311–318. doi:10.​1007/​s10753-004-6641-z CrossRefPubMed
18.
Zurück zum Zitat McGraw WT, Potempa J, Farley D, Travis J (1999) Purification, characterization, and sequence analysis of a potential virulence factor from Porphyromonas gingivalis, peptidylarginine deiminase. Infect Immun 67:3248–3256PubMedPubMedCentral McGraw WT, Potempa J, Farley D, Travis J (1999) Purification, characterization, and sequence analysis of a potential virulence factor from Porphyromonas gingivalis, peptidylarginine deiminase. Infect Immun 67:3248–3256PubMedPubMedCentral
19.
Zurück zum Zitat Goulas T, Mizgalska D, Garcia-Ferrer I, Kantyka T, Guevara T, Szmigielski B, Sroka A, Millan C, Uson I, Veillard F, Potempa B, Mydel P, Sola M, Potempa J, Gomis-Ruth FX (2015) Structure and mechanism of a bacterial host-protein citrullinating virulence factor, Porphyromonas gingivalis peptidylarginine deiminase. Sci Rep 5:11969. doi:10.1038/srep11969 CrossRefPubMedPubMedCentral Goulas T, Mizgalska D, Garcia-Ferrer I, Kantyka T, Guevara T, Szmigielski B, Sroka A, Millan C, Uson I, Veillard F, Potempa B, Mydel P, Sola M, Potempa J, Gomis-Ruth FX (2015) Structure and mechanism of a bacterial host-protein citrullinating virulence factor, Porphyromonas gingivalis peptidylarginine deiminase. Sci Rep 5:11969. doi:10.​1038/​srep11969 CrossRefPubMedPubMedCentral
20.
Zurück zum Zitat Wegner N, Wait R, Sroka A, Eick S, Nguyen KA, Lundberg K, Kinloch A, Culshaw S, Potempa J, Venables PJ (2010) Peptidylarginine deiminase from Porphyromonas gingivalis citrullinates human fibrinogen and alpha-enolase: implications for autoimmunity in rheumatoid arthritis. Arthritis Rheum 62:2662–2672. doi:10.1002/art.27552 CrossRefPubMedPubMedCentral Wegner N, Wait R, Sroka A, Eick S, Nguyen KA, Lundberg K, Kinloch A, Culshaw S, Potempa J, Venables PJ (2010) Peptidylarginine deiminase from Porphyromonas gingivalis citrullinates human fibrinogen and alpha-enolase: implications for autoimmunity in rheumatoid arthritis. Arthritis Rheum 62:2662–2672. doi:10.​1002/​art.​27552 CrossRefPubMedPubMedCentral
22.
Zurück zum Zitat Hitchon CA, Chandad F, Ferucci ED, Willemze A, Ioan-Facsinay A, van der Woude D, Markland J, Robinson D, Elias B, Newkirk M, Toes RM, Huizinga TW, El-Gabalawy HS (2010) Antibodies to Porphyromonas gingivalis are associated with anticitrullinated protein antibodies in patients with rheumatoid arthritis and their relatives. J Rheumatol 37:1105–1112 doi: jrheum.091323 [pii]CrossRefPubMed Hitchon CA, Chandad F, Ferucci ED, Willemze A, Ioan-Facsinay A, van der Woude D, Markland J, Robinson D, Elias B, Newkirk M, Toes RM, Huizinga TW, El-Gabalawy HS (2010) Antibodies to Porphyromonas gingivalis are associated with anticitrullinated protein antibodies in patients with rheumatoid arthritis and their relatives. J Rheumatol 37:1105–1112 doi: jrheum.091323 [pii]CrossRefPubMed
23.
Zurück zum Zitat Aletaha D, Neogi T, Silman AJ, Funovits J, Felson DT, Bingham CO 3rd, Birnbaum NS, Burmester GR, Bykerk VP, Cohen MD, Combe B, Costenbader KH, Dougados M, Emery P, Ferraccioli G, Hazes JM, Hobbs K, Huizinga TW, Kavanaugh A, Kay J, Kvien TK, Laing T, Mease P, Menard HA, Moreland LW, Naden RL, Pincus T, Smolen JS, Stanislawska-Biernat E, Symmons D, Tak PP, Upchurch KS, Vencovsky J, Wolfe F, Hawker G (2010) Rheumatoid arthritis classification criteria: an American College of Rheumatology/European league against rheumatism collaborative initiative. Arthritis Rheum 62:2569–2581. doi:10.1002/art.27584 CrossRefPubMed Aletaha D, Neogi T, Silman AJ, Funovits J, Felson DT, Bingham CO 3rd, Birnbaum NS, Burmester GR, Bykerk VP, Cohen MD, Combe B, Costenbader KH, Dougados M, Emery P, Ferraccioli G, Hazes JM, Hobbs K, Huizinga TW, Kavanaugh A, Kay J, Kvien TK, Laing T, Mease P, Menard HA, Moreland LW, Naden RL, Pincus T, Smolen JS, Stanislawska-Biernat E, Symmons D, Tak PP, Upchurch KS, Vencovsky J, Wolfe F, Hawker G (2010) Rheumatoid arthritis classification criteria: an American College of Rheumatology/European league against rheumatism collaborative initiative. Arthritis Rheum 62:2569–2581. doi:10.​1002/​art.​27584 CrossRefPubMed
24.
Zurück zum Zitat Arnett FC, Edworthy SM, Bloch DA, McShane DJ, Fries JF, Cooper NS, Healey LA, Kaplan SR, Liang MH, Luthra HS, et al. (1988) The American rheumatism association 1987 revised criteria for the classification of rheumatoid arthritis. Arthritis Rheum 31:315–324CrossRefPubMed Arnett FC, Edworthy SM, Bloch DA, McShane DJ, Fries JF, Cooper NS, Healey LA, Kaplan SR, Liang MH, Luthra HS, et al. (1988) The American rheumatism association 1987 revised criteria for the classification of rheumatoid arthritis. Arthritis Rheum 31:315–324CrossRefPubMed
25.
Zurück zum Zitat SAS Institute Inc. SAS/STAT® (2013) User’s Guide. Version 9.4. SAS Institute Inc., Cary, NC SAS Institute Inc. SAS/STAT® (2013) User’s Guide. Version 9.4. SAS Institute Inc., Cary, NC
26.
Zurück zum Zitat Yusof Z, Porter SR, Greenman J, Scully C (1995) Levels of serum IgG against Porphyromonas gingivalis in patients with rapidly progressive periodontitis, rheumatoid arthritis and adult periodontitis. J Nihon Univ Sch Dent 37:197–200CrossRefPubMed Yusof Z, Porter SR, Greenman J, Scully C (1995) Levels of serum IgG against Porphyromonas gingivalis in patients with rapidly progressive periodontitis, rheumatoid arthritis and adult periodontitis. J Nihon Univ Sch Dent 37:197–200CrossRefPubMed
27.
Zurück zum Zitat Moen K, Brun JG, Madland TM, Tynning T, Jonsson R (2003) Immunoglobulin G and a antibody responses to Bacteroides forsythus and Prevotella intermedia in sera and synovial fluids of arthritis patients. Clin Diagn Lab Immunol 10:1043–1050PubMedPubMedCentral Moen K, Brun JG, Madland TM, Tynning T, Jonsson R (2003) Immunoglobulin G and a antibody responses to Bacteroides forsythus and Prevotella intermedia in sera and synovial fluids of arthritis patients. Clin Diagn Lab Immunol 10:1043–1050PubMedPubMedCentral
28.
Zurück zum Zitat Ogrendik M, Kokino S, Ozdemir F, Bird PS, Hamlet S (2005) Serum antibodies to oral anaerobic bacteria in patients with rheumatoid arthritis. MedGenMed 7:2 doi: 505458 [pii]PubMedPubMedCentral Ogrendik M, Kokino S, Ozdemir F, Bird PS, Hamlet S (2005) Serum antibodies to oral anaerobic bacteria in patients with rheumatoid arthritis. MedGenMed 7:2 doi: 505458 [pii]PubMedPubMedCentral
29.
Zurück zum Zitat Okada M, Kobayashi T, Ito S, Yokoyama T, Komatsu Y, Abe A, Murasawa A, Yoshie H (2011) Antibody responses to periodontopathic bacteria in relation to rheumatoid arthritis in Japanese adults. J Periodontol 82:1433–1441. doi:10.1902/jop.2011.110020 CrossRefPubMed Okada M, Kobayashi T, Ito S, Yokoyama T, Komatsu Y, Abe A, Murasawa A, Yoshie H (2011) Antibody responses to periodontopathic bacteria in relation to rheumatoid arthritis in Japanese adults. J Periodontol 82:1433–1441. doi:10.​1902/​jop.​2011.​110020 CrossRefPubMed
30.
Zurück zum Zitat Arvikar SL, Collier DS, Fisher MC, Unizony S, Cohen GL, McHugh G, Kawai T, Strle K, Steere AC (2013) Clinical correlations with Porphyromonas gingivalis antibody responses in patients with early rheumatoid arthritis. Arthritis Res Ther 15:R109 doi: ar4289 [pii]CrossRefPubMedPubMedCentral Arvikar SL, Collier DS, Fisher MC, Unizony S, Cohen GL, McHugh G, Kawai T, Strle K, Steere AC (2013) Clinical correlations with Porphyromonas gingivalis antibody responses in patients with early rheumatoid arthritis. Arthritis Res Ther 15:R109 doi: ar4289 [pii]CrossRefPubMedPubMedCentral
31.
Zurück zum Zitat Laugisch O, Wong A, Sroka A, Kantyka T, Koziel J, Neuhaus K, Sculean A, Venables PJ, Potempa J, Moller B, Eick S (2015) Citrullination in the periodontium-a possible link between periodontitis and rheumatoid arthritis. Clin Oral Investig. doi:10.1007/s00784-015-1556-7 PubMed Laugisch O, Wong A, Sroka A, Kantyka T, Koziel J, Neuhaus K, Sculean A, Venables PJ, Potempa J, Moller B, Eick S (2015) Citrullination in the periodontium-a possible link between periodontitis and rheumatoid arthritis. Clin Oral Investig. doi:10.​1007/​s00784-015-1556-7 PubMed
32.
Zurück zum Zitat Quirke AM, Lugli EB, Wegner N, Hamilton BC, Charles P, Chowdhury M, Ytterberg AJ, Zubarev RA, Potempa J, Culshaw S, Guo Y, Fisher BA, Thiele G, Mikuls TR, Venables PJ (2014) Heightened immune response to autocitrullinated Porphyromonas gingivalis peptidylarginine deiminase: a potential mechanism for breaching immunologic tolerance in rheumatoid arthritis. Ann Rheum Dis 73:263–269. doi:10.1136/annrheumdis-2012-202726 [pii]CrossRefPubMed Quirke AM, Lugli EB, Wegner N, Hamilton BC, Charles P, Chowdhury M, Ytterberg AJ, Zubarev RA, Potempa J, Culshaw S, Guo Y, Fisher BA, Thiele G, Mikuls TR, Venables PJ (2014) Heightened immune response to autocitrullinated Porphyromonas gingivalis peptidylarginine deiminase: a potential mechanism for breaching immunologic tolerance in rheumatoid arthritis. Ann Rheum Dis 73:263–269. doi:10.​1136/​annrheumdis-2012-202726 [pii]CrossRefPubMed
33.
Zurück zum Zitat Konig MF, Paracha AS, Moni M, Bingham CO 3rd, Andrade F (2015) Defining the role of Porphyromonas gingivalis peptidylarginine deiminase (PPAD) in rheumatoid arthritis through the study of PPAD biology. Ann Rheum Dis 74:2054–2061. doi:10.1136/annrheumdis-2014-205385 CrossRefPubMed Konig MF, Paracha AS, Moni M, Bingham CO 3rd, Andrade F (2015) Defining the role of Porphyromonas gingivalis peptidylarginine deiminase (PPAD) in rheumatoid arthritis through the study of PPAD biology. Ann Rheum Dis 74:2054–2061. doi:10.​1136/​annrheumdis-2014-205385 CrossRefPubMed
34.
Zurück zum Zitat Kharlamova N, Jiang X, Sherina N, Potempa B, Israelsson L, Quirke AM, Eriksson K, Yucel-Lindberg T, Venables PJ, Potempa J, Alfredsson L, Lundberg K (2015) Antibodies to Porphyromonas gingivalis indicate interaction between oral infection, smoking and risk genes in rheumatoid arthritis etiology. Arthritis Rheumatol. doi:10.1002/art.39491 Kharlamova N, Jiang X, Sherina N, Potempa B, Israelsson L, Quirke AM, Eriksson K, Yucel-Lindberg T, Venables PJ, Potempa J, Alfredsson L, Lundberg K (2015) Antibodies to Porphyromonas gingivalis indicate interaction between oral infection, smoking and risk genes in rheumatoid arthritis etiology. Arthritis Rheumatol. doi:10.​1002/​art.​39491
35.
Zurück zum Zitat Lee JY, Choi IA, Kim JH, Kim KH, Lee EY, Lee EB, Lee YM, Song YW (2015) Association between anti-Porphyromonas gingivalis or anti-alpha-enolase antibody and severity of periodontitis or rheumatoid arthritis (RA) disease activity in RA. BMC Musculoskelet Disord 16:190. doi:10.1186/s12891-015-0647-6 CrossRefPubMedPubMedCentral Lee JY, Choi IA, Kim JH, Kim KH, Lee EY, Lee EB, Lee YM, Song YW (2015) Association between anti-Porphyromonas gingivalis or anti-alpha-enolase antibody and severity of periodontitis or rheumatoid arthritis (RA) disease activity in RA. BMC Musculoskelet Disord 16:190. doi:10.​1186/​s12891-015-0647-6 CrossRefPubMedPubMedCentral
36.
Zurück zum Zitat Seror R, Le Gall-David S, Bonnaure-Mallet M, Schaeverbeke T, Cantagrel A, Minet J, Gottenberg JE, Chanson P, Ravaud P, Mariette X (2015) Association of Anti-Porphyromonas gingivalis antibody titers with nonsmoking status in early rheumatoid arthritis: results from the prospective French cohort of patients with early rheumatoid arthritis. Arthritis Rheumatol 67:1729–1737. doi:10.1002/art.39118 CrossRefPubMed Seror R, Le Gall-David S, Bonnaure-Mallet M, Schaeverbeke T, Cantagrel A, Minet J, Gottenberg JE, Chanson P, Ravaud P, Mariette X (2015) Association of Anti-Porphyromonas gingivalis antibody titers with nonsmoking status in early rheumatoid arthritis: results from the prospective French cohort of patients with early rheumatoid arthritis. Arthritis Rheumatol 67:1729–1737. doi:10.​1002/​art.​39118 CrossRefPubMed
37.
Zurück zum Zitat Shimada A, Kobayashi T, Ito S, Okada M, Murasawa A, Nakazono K, Yoshie H (2016) Expression of anti-Porphyromonas gingivalis peptidylarginine deiminase immunoglobulin G and peptidylarginine deiminase-4 in patients with rheumatoid arthritis and periodontitis. J Periodontal Res 51:103–111. doi:10.1111/jre.12288 CrossRefPubMed Shimada A, Kobayashi T, Ito S, Okada M, Murasawa A, Nakazono K, Yoshie H (2016) Expression of anti-Porphyromonas gingivalis peptidylarginine deiminase immunoglobulin G and peptidylarginine deiminase-4 in patients with rheumatoid arthritis and periodontitis. J Periodontal Res 51:103–111. doi:10.​1111/​jre.​12288 CrossRefPubMed
39.
Zurück zum Zitat Mikuls TR, Thiele GM, Deane KD, Payne JB, O'Dell JR, Yu F, Sayles H, Weisman MH, Gregersen PK, Buckner JH, Keating RM, Derber LA, Robinson WH, Holers VM, Norris JM (2012) Porphyromonas gingivalis and disease-related autoantibodies in individuals at increased risk of rheumatoid arthritis. Arthritis Rheum 64:3522–3530. doi:10.1002/art.34595 CrossRefPubMed Mikuls TR, Thiele GM, Deane KD, Payne JB, O'Dell JR, Yu F, Sayles H, Weisman MH, Gregersen PK, Buckner JH, Keating RM, Derber LA, Robinson WH, Holers VM, Norris JM (2012) Porphyromonas gingivalis and disease-related autoantibodies in individuals at increased risk of rheumatoid arthritis. Arthritis Rheum 64:3522–3530. doi:10.​1002/​art.​34595 CrossRefPubMed
41.
Zurück zum Zitat de Smit M, Westra J, Vissink A, Doornbos-van der Meer B, Brouwer E, van Winkelhoff AJ (2012) Periodontitis in established rheumatoid arthritis patients: a cross-sectional clinical, microbiological and serological study. Arthritis Res Ther 14:R222. doi:10.1186/ar4061 CrossRefPubMedPubMedCentral de Smit M, Westra J, Vissink A, Doornbos-van der Meer B, Brouwer E, van Winkelhoff AJ (2012) Periodontitis in established rheumatoid arthritis patients: a cross-sectional clinical, microbiological and serological study. Arthritis Res Ther 14:R222. doi:10.​1186/​ar4061 CrossRefPubMedPubMedCentral
42.
Zurück zum Zitat Lappin DF, Apatzidou D, Quirke AM, Oliver-Bell J, Butcher JP, Kinane DF, Riggio MP, Venables P, McInnes IB, Culshaw S (2013) Influence of periodontal disease, Porphyromonas gingivalis and cigarette smoking on systemic anti-citrullinated peptide antibody titres. J Clin Periodontol 40:907–915. doi:10.1111/jcpe.12138 CrossRefPubMed Lappin DF, Apatzidou D, Quirke AM, Oliver-Bell J, Butcher JP, Kinane DF, Riggio MP, Venables P, McInnes IB, Culshaw S (2013) Influence of periodontal disease, Porphyromonas gingivalis and cigarette smoking on systemic anti-citrullinated peptide antibody titres. J Clin Periodontol 40:907–915. doi:10.​1111/​jcpe.​12138 CrossRefPubMed
43.
Zurück zum Zitat Okada M, Kobayashi T, Ito S, Yokoyama T, Abe A, Murasawa A, Yoshie H (2013) Periodontal treatment decreases levels of antibodies to Porphyromonas gingivalis and citrulline in patients with rheumatoid arthritis and periodontitis. J Periodontol 84:e74–e84. doi:10.1902/jop.2013.130079 CrossRefPubMed Okada M, Kobayashi T, Ito S, Yokoyama T, Abe A, Murasawa A, Yoshie H (2013) Periodontal treatment decreases levels of antibodies to Porphyromonas gingivalis and citrulline in patients with rheumatoid arthritis and periodontitis. J Periodontol 84:e74–e84. doi:10.​1902/​jop.​2013.​130079 CrossRefPubMed
44.
Zurück zum Zitat Kobayashi T, Okada M, Ito S, Kobayashi D, Ishida K, Kojima A, Narita I, Murasawa A, Yoshie H (2014) Assessment of interleukin-6 receptor inhibition therapy on periodontal condition in patients with rheumatoid arthritis and chronic periodontitis. J Periodontol 85:57–67. doi:10.1902/jop.2013.120696 CrossRefPubMed Kobayashi T, Okada M, Ito S, Kobayashi D, Ishida K, Kojima A, Narita I, Murasawa A, Yoshie H (2014) Assessment of interleukin-6 receptor inhibition therapy on periodontal condition in patients with rheumatoid arthritis and chronic periodontitis. J Periodontol 85:57–67. doi:10.​1902/​jop.​2013.​120696 CrossRefPubMed
45.
Zurück zum Zitat Mikuls TR, Payne JB, Yu F, Thiele GM, Reynolds RJ, Cannon GW, Markt J, McGowan D, Kerr GS, Redman RS, Reimold A, Griffiths G, Beatty M, Gonzalez SM, Bergman DA, Hamilton BC 3rd, Erickson AR, Sokolove J, Robinson WH, Walker C, Chandad F, O'Dell JR (2014) Periodontitis and Porphyromonas gingivalis in patients with rheumatoid arthritis. Arthritis Rheumatol 66:1090–1100. doi:10.1002/art.38348 CrossRefPubMedPubMedCentral Mikuls TR, Payne JB, Yu F, Thiele GM, Reynolds RJ, Cannon GW, Markt J, McGowan D, Kerr GS, Redman RS, Reimold A, Griffiths G, Beatty M, Gonzalez SM, Bergman DA, Hamilton BC 3rd, Erickson AR, Sokolove J, Robinson WH, Walker C, Chandad F, O'Dell JR (2014) Periodontitis and Porphyromonas gingivalis in patients with rheumatoid arthritis. Arthritis Rheumatol 66:1090–1100. doi:10.​1002/​art.​38348 CrossRefPubMedPubMedCentral
46.
Zurück zum Zitat de Smit M, van de Stadt LA, Janssen KM, Doornbos-van der Meer B, Vissink A, van Winkelhoff AJ, Brouwer E, Westra J, van Schaardenburg D (2014) Antibodies against Porphyromonas gingivalis in seropositive arthralgia patients do not predict development of rheumatoid arthritis. Ann Rheum Dis 73:1277–1279. doi:10.1136/annrheumdis-2013-204594 CrossRefPubMed de Smit M, van de Stadt LA, Janssen KM, Doornbos-van der Meer B, Vissink A, van Winkelhoff AJ, Brouwer E, Westra J, van Schaardenburg D (2014) Antibodies against Porphyromonas gingivalis in seropositive arthralgia patients do not predict development of rheumatoid arthritis. Ann Rheum Dis 73:1277–1279. doi:10.​1136/​annrheumdis-2013-204594 CrossRefPubMed
47.
Zurück zum Zitat Kimura Y, Yoshida S, Takeuchi T, Kimura M, Yoshikawa A, Hiramatsu Y, Ishida T, Makino S, Takasugi Y, Hanafusa T (2015) Periodontal pathogens participate in synovitis in patients with rheumatoid arthritis in clinical remission: a retrospective case-control study. Rheumatology (Oxford) 54:2257–2263. doi:10.1093/rheumatology/kev274 Kimura Y, Yoshida S, Takeuchi T, Kimura M, Yoshikawa A, Hiramatsu Y, Ishida T, Makino S, Takasugi Y, Hanafusa T (2015) Periodontal pathogens participate in synovitis in patients with rheumatoid arthritis in clinical remission: a retrospective case-control study. Rheumatology (Oxford) 54:2257–2263. doi:10.​1093/​rheumatology/​kev274
48.
Zurück zum Zitat Janssen KM, de Smit MJ, Brouwer E, de Kok FA, Kraan J, Altenburg J, Verheul MK, Trouw LA, van Winkelhoff AJ, Vissink A, Westra J (2015) Rheumatoid arthritis-associated autoantibodies in non-rheumatoid arthritis patients with mucosal inflammation: a case-control study. Arthritis research & therapy 17:174. doi:10.1186/s13075-015-0690-6 CrossRef Janssen KM, de Smit MJ, Brouwer E, de Kok FA, Kraan J, Altenburg J, Verheul MK, Trouw LA, van Winkelhoff AJ, Vissink A, Westra J (2015) Rheumatoid arthritis-associated autoantibodies in non-rheumatoid arthritis patients with mucosal inflammation: a case-control study. Arthritis research & therapy 17:174. doi:10.​1186/​s13075-015-0690-6 CrossRef
49.
Zurück zum Zitat Bello-Gualtero JM, Lafaurie GI, Hoyos LX, Castillo DM, De-Avila J, Munevar JC, Unriza S, Londono J, Valle-Onate R, Romero-Sanchez C (2015) Periodontal disease in individuals with a genetic risk of developing arthritis or with early rheumatoid arthritis: a cross-sectional study. J Periodontol:1–18. doi:10.1902/jop.2015.150455 Bello-Gualtero JM, Lafaurie GI, Hoyos LX, Castillo DM, De-Avila J, Munevar JC, Unriza S, Londono J, Valle-Onate R, Romero-Sanchez C (2015) Periodontal disease in individuals with a genetic risk of developing arthritis or with early rheumatoid arthritis: a cross-sectional study. J Periodontol:1–18. doi:10.​1902/​jop.​2015.​150455
50.
Zurück zum Zitat Reichert S, Schlumberger W, Dahnrich C, Hornig N, Altermann W, Schaller HG, Schulz S (2015) Association of levels of antibodies against citrullinated cyclic peptides and citrullinated alpha-enolase in chronic and aggressive periodontitis as a risk factor of rheumatoid arthritis: a case control study. J Transl Med 13:283. doi:10.1186/s12967-015-0625-7 CrossRefPubMedPubMedCentral Reichert S, Schlumberger W, Dahnrich C, Hornig N, Altermann W, Schaller HG, Schulz S (2015) Association of levels of antibodies against citrullinated cyclic peptides and citrullinated alpha-enolase in chronic and aggressive periodontitis as a risk factor of rheumatoid arthritis: a case control study. J Transl Med 13:283. doi:10.​1186/​s12967-015-0625-7 CrossRefPubMedPubMedCentral
51.
Zurück zum Zitat Fisher BA, Cartwright AJ, Quirke AM, de Pablo P, Romaguera D, Panico S, Mattiello A, Gavrila D, Navarro C, Sacerdote C, Vineis P, Tumino R, Lappin DF, Apazidou D, Culshaw S, Potempa J, Michaud DS, Riboli E, Venables PJ (2015) Smoking, Porphyromonas gingivalis and the immune response to citrullinated autoantigens before the clinical onset of rheumatoid arthritis in a southern European nested case-control study. BMC Musculoskelet Disord 16:331. doi:10.1186/s12891-015-0792-y CrossRefPubMedPubMedCentral Fisher BA, Cartwright AJ, Quirke AM, de Pablo P, Romaguera D, Panico S, Mattiello A, Gavrila D, Navarro C, Sacerdote C, Vineis P, Tumino R, Lappin DF, Apazidou D, Culshaw S, Potempa J, Michaud DS, Riboli E, Venables PJ (2015) Smoking, Porphyromonas gingivalis and the immune response to citrullinated autoantigens before the clinical onset of rheumatoid arthritis in a southern European nested case-control study. BMC Musculoskelet Disord 16:331. doi:10.​1186/​s12891-015-0792-y CrossRefPubMedPubMedCentral
54.
Zurück zum Zitat Singh A, Wyant T, Anaya-Bergman C, Aduse-Opoku J, Brunner J, Laine ML, Curtis MA, Lewis JP (2011) The capsule of Porphyromonas gingivalis leads to a reduction in the host inflammatory response, evasion of phagocytosis, and increase in virulence. Infect Immun 79:4533–4542. doi:10.1128/IAI.05016-11 CrossRefPubMedPubMedCentral Singh A, Wyant T, Anaya-Bergman C, Aduse-Opoku J, Brunner J, Laine ML, Curtis MA, Lewis JP (2011) The capsule of Porphyromonas gingivalis leads to a reduction in the host inflammatory response, evasion of phagocytosis, and increase in virulence. Infect Immun 79:4533–4542. doi:10.​1128/​IAI.​05016-11 CrossRefPubMedPubMedCentral
56.
Zurück zum Zitat Liljestrand JM, Gursoy UK, Hyvarinen K, Sorsa T, Suominen AL, Kononen E, Pussinen PJ (2014) Combining salivary pathogen and serum antibody levels improves their diagnostic ability in detection of periodontitis. J Periodontol 85:123–131. doi:10.1902/jop.2013.130030 CrossRefPubMed Liljestrand JM, Gursoy UK, Hyvarinen K, Sorsa T, Suominen AL, Kononen E, Pussinen PJ (2014) Combining salivary pathogen and serum antibody levels improves their diagnostic ability in detection of periodontitis. J Periodontol 85:123–131. doi:10.​1902/​jop.​2013.​130030 CrossRefPubMed
58.
Zurück zum Zitat Kudo C, Naruishi K, Maeda H, Abiko Y, Hino T, Iwata M, Mitsuhashi C, Murakami S, Nagasawa T, Nagata T, Yoneda S, Nomura Y, Noguchi T, Numabe Y, Ogata Y, Sato T, Shimauchi H, Yamazaki K, Yoshimura A, Takashiba S (2012) Assessment of the plasma/serum IgG test to screen for periodontitis. J Dent Res 91:1190–1195. doi:10.1177/0022034512461796 [pii]CrossRefPubMed Kudo C, Naruishi K, Maeda H, Abiko Y, Hino T, Iwata M, Mitsuhashi C, Murakami S, Nagasawa T, Nagata T, Yoneda S, Nomura Y, Noguchi T, Numabe Y, Ogata Y, Sato T, Shimauchi H, Yamazaki K, Yoshimura A, Takashiba S (2012) Assessment of the plasma/serum IgG test to screen for periodontitis. J Dent Res 91:1190–1195. doi:10.​1177/​0022034512461796​ [pii]CrossRefPubMed
59.
Zurück zum Zitat Dye BA, Herrera-Abreu M, Lerche-Sehm J, Vlachojannis C, Pikdoken L, Pretzl B, Schwartz A, Papapanou PN (2009) Serum antibodies to periodontal bacteria as diagnostic markers of periodontitis. J Periodontol 80:634–647. doi:10.1902/jop.2009.080474 CrossRefPubMed Dye BA, Herrera-Abreu M, Lerche-Sehm J, Vlachojannis C, Pikdoken L, Pretzl B, Schwartz A, Papapanou PN (2009) Serum antibodies to periodontal bacteria as diagnostic markers of periodontitis. J Periodontol 80:634–647. doi:10.​1902/​jop.​2009.​080474 CrossRefPubMed
60.
Zurück zum Zitat Hosaka Y, Saito A, Nakagawa T, Seida K, Yamada S, Okuda K (1994) Effect of initial therapy on dynamics of immunogloblin G levels to some periodontopathic bacteria in serum and gingival crevicular fluid. Bull Tokyo Dent Coll 35:207–216PubMed Hosaka Y, Saito A, Nakagawa T, Seida K, Yamada S, Okuda K (1994) Effect of initial therapy on dynamics of immunogloblin G levels to some periodontopathic bacteria in serum and gingival crevicular fluid. Bull Tokyo Dent Coll 35:207–216PubMed
61.
Zurück zum Zitat Lamont RJ, Hajishengallis GN, Jenkinson HF (2014) Oral microbiology and immunology, 2nd edn . ASM Press, WashingtonBook title Lamont RJ, Hajishengallis GN, Jenkinson HF (2014) Oral microbiology and immunology, 2nd edn . ASM Press, WashingtonBook title
62.
Zurück zum Zitat Curtis MA, Slaney JM, Carman RJ, Johnson NW (1991) Identification of the major surface protein antigens of Porphyromonas gingivalis using IgG antibody reactivity of periodontal case-control serum. Oral Microbiol Immunol 6:321–326CrossRefPubMed Curtis MA, Slaney JM, Carman RJ, Johnson NW (1991) Identification of the major surface protein antigens of Porphyromonas gingivalis using IgG antibody reactivity of periodontal case-control serum. Oral Microbiol Immunol 6:321–326CrossRefPubMed
63.
Zurück zum Zitat Konig MF, Paracha AS, Moni M, Bingham CO, 3rd and Andrade F (2014) Defining the role of Porphyromonas gingivalis peptidylarginine deiminase (PPAD) in rheumatoid arthritis through the study of PPAD biology. Ann Rheum Dis. doi: annrheumdis-2014-205385 [pii] Konig MF, Paracha AS, Moni M, Bingham CO, 3rd and Andrade F (2014) Defining the role of Porphyromonas gingivalis peptidylarginine deiminase (PPAD) in rheumatoid arthritis through the study of PPAD biology. Ann Rheum Dis. doi: annrheumdis-2014-205385 [pii]
64.
Zurück zum Zitat Hanaoka Y, Soejima H, Yasuda O, Nakayama H, Nagata M, Matsuo K, Shinohara M, Izumi Y, Ogawa H (2013) Level of serum antibody against a periodontal pathogen is associated with atherosclerosis and hypertension. Hypertens Res 36:829–833. doi:10.1038/hr.2013.46 [pii]CrossRefPubMed Hanaoka Y, Soejima H, Yasuda O, Nakayama H, Nagata M, Matsuo K, Shinohara M, Izumi Y, Ogawa H (2013) Level of serum antibody against a periodontal pathogen is associated with atherosclerosis and hypertension. Hypertens Res 36:829–833. doi:10.​1038/​hr.​2013.​46 [pii]CrossRefPubMed
65.
Zurück zum Zitat Arbes SJ Jr, Sever ML, Vaughn B, Cohen EA, Zeldin DC (2006) Oral pathogens and allergic disease: results from the third National Health and nutrition examination survey. J Allergy Clin Immunol 118:1169–1175. doi:10.1016/j.jaci.2006.07.029 S0091-6749(06)01578-8 Arbes SJ Jr, Sever ML, Vaughn B, Cohen EA, Zeldin DC (2006) Oral pathogens and allergic disease: results from the third National Health and nutrition examination survey. J Allergy Clin Immunol 118:1169–1175. doi:10.​1016/​j.​jaci.​2006.​07.​029 S0091-6749(06)01578-8
68.
69.
Zurück zum Zitat Pons-Fuster A, Rodriguez Agudo C, Galvez Munoz P, Saiz Cuenca E, Pina Perez FM, Lopez-Jornet P (2015) Clinical evaluation of periodontal disease in patients with rheumatoid arthritis: a cross-sectional study. Quintessence Int. doi:10.3290/j.qi.a34456 Pons-Fuster A, Rodriguez Agudo C, Galvez Munoz P, Saiz Cuenca E, Pina Perez FM, Lopez-Jornet P (2015) Clinical evaluation of periodontal disease in patients with rheumatoid arthritis: a cross-sectional study. Quintessence Int. doi:10.​3290/​j.​qi.​a34456
Metadaten
Titel
Serum antibody levels against Porphyromonas gingivalis in patients with and without rheumatoid arthritis – a systematic review and meta-analysis
verfasst von
Philip Bender
Walter B. Bürgin
Anton Sculean
Sigrun Eick
Publikationsdatum
25.08.2016
Verlag
Springer Berlin Heidelberg
Erschienen in
Clinical Oral Investigations / Ausgabe 1/2017
Print ISSN: 1432-6981
Elektronische ISSN: 1436-3771
DOI
https://doi.org/10.1007/s00784-016-1938-5

Weitere Artikel der Ausgabe 1/2017

Clinical Oral Investigations 1/2017 Zur Ausgabe

Parodontalbehandlung verbessert Prognose bei Katheterablation

19.04.2024 Vorhofflimmern Nachrichten

Werden Personen mit Vorhofflimmern in der Blanking-Periode nach einer Katheterablation gegen eine bestehende Parodontitis behandelt, verbessert dies die Erfolgsaussichten. Dafür sprechen die Resultate einer prospektiven Untersuchung.

Invasive Zahnbehandlung: Wann eine Antibiotikaprophylaxe vor infektiöser Endokarditis schützt

11.04.2024 Endokarditis Nachrichten

Bei welchen Personen eine Antibiotikaprophylaxe zur Prävention einer infektiösen Endokarditis nach invasiven zahnärztlichen Eingriffen sinnvoll ist, wird diskutiert. Neue Daten stehen im Einklang mit den europäischen Leitlinienempfehlungen.

Zell-Organisatoren unter Druck: Mechanismen des embryonalen Zahnwachstums aufgedeckt

08.04.2024 Zahnmedizin Nachrichten

Der Aufbau von Geweben und Organen während der Embryonalentwicklung wird von den Zellen bemerkenswert choreografiert. Für diesen Prozess braucht es spezielle sogenannte „Organisatoren“. In einer aktuellen Veröffentlichung im Fachjournal Nature Cell Biology berichten Forschende durch welchen Vorgang diese Organisatoren im Gewebe entstehen und wie sie dann die Bildung von Zähnen orchestrieren.

Die Oralprophylaxe & Kinderzahnheilkunde umbenannt

11.03.2024 Kinderzahnmedizin Nachrichten

Infolge der Umbenennung der Deutschen Gesellschaft für Kinderzahnheilkunde in Deutsche Gesellschaft für Kinderzahnmedizin (DGKiZ) wird deren Mitgliederzeitschrift Oralprophylaxe & Kinderzahnheilkunde in Oralprophylaxe & Kinderzahnmedizin umbenannt. Aus diesem Grunde trägt die erste Ausgabe in 2024 erstmalig den neuen Titel.

Newsletter

Bestellen Sie unseren kostenlosen Newsletter Update Zahnmedizin und bleiben Sie gut informiert – ganz bequem per eMail.