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Published in: Arthritis Research & Therapy 1/2019

Open Access 01-12-2019 | Rheumatoid Arthritis | Research article

Association between severity of periodontitis and clinical activity in rheumatoid arthritis patients: a case–control study

Authors: Beatriz Rodríguez-Lozano, Jerián González-Febles, Jorge Luis Garnier-Rodríguez, Shashi Dadlani, Sagrario Bustabad-Reyes, Mariano Sanz, Fernando Sánchez-Alonso, Carlos Sánchez-Piedra, Enrique González-Dávila, Federico Díaz-González

Published in: Arthritis Research & Therapy | Issue 1/2019

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Abstract

Background

A high prevalence of periodontitis has been reported in rheumatoid arthritis (RA) patients, although the strength of this association, its temporal link and the possible relationship between the severity of periodontitis and RA disease activity remain unclear. The objective of this work was to investigate whether periodontitis is associated with RA and whether periodontitis severity is linked to RA disease activity.

Methods

This case–control study included 187 patients diagnosed with RA and 157 control patients without inflammatory joint disease. RA disease activity and severity were evaluated by the Disease Activity Score 28, the Simplified Disease Activity Index, the Clinical Disease Activity Index, rheumatoid factor, anti-citrullinated protein antibody titers, the erythrocyte sedimentation rate, C-reactive protein, presence of extra-articular manifestations and type of RA therapy. Exposure severity was assessed by the following periodontal parameters: plaque index, bleeding on probing, probing pocket depth and clinical attachment levels. Sociodemographic variables and comorbidities were evaluated as confounding variables. Outcome and exposure variables were compared by both parametric and nonparametric tests, and possible associations were assessed through regression analysis with a calculation for the adjusted odds ratio (OR).

Results

A significant association was demonstrated between periodontitis and RA with an adjusted OR of 20.57 (95% CI 6.02–70.27, p < 0.001). Compared with controls, all parameters related to periodontal status (plaque index, bleeding on probing, probing pocket depth and clinical attachment levels) were significantly worse in RA patients (p < 0.001). Periodontitis severity was significantly associated with RA disease activity (p < 0.001), showing in an ordinal logistic regression model an association between periodontal severity and disease activity with an adjusted OR of 2.66 (95% CI 1.24–5.74, p = 0.012).

Conclusion

A significant association was demonstrated between periodontitis and RA, independent of other confounders. This association was more evident in patients with pronounced periodontal disease and higher RA disease activity.
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Literature
1.
go back to reference Avina-Zubieta JA, Choi HK, Sadatsafavi M, Etminan M, Esdaile JM, Lacaille D. Risk of cardiovascular mortality in patients with rheumatoid arthritis: a meta-analysis of observational studies. Arthritis Rheum. 2008;59:1690–7.CrossRef Avina-Zubieta JA, Choi HK, Sadatsafavi M, Etminan M, Esdaile JM, Lacaille D. Risk of cardiovascular mortality in patients with rheumatoid arthritis: a meta-analysis of observational studies. Arthritis Rheum. 2008;59:1690–7.CrossRef
2.
go back to reference de Pablo P, Chapple IL, Buckley CD, Dietrich T. Periodontitis in systemic rheumatic diseases. Nat Rev Rheumatol. 2009;5:218–24.CrossRef de Pablo P, Chapple IL, Buckley CD, Dietrich T. Periodontitis in systemic rheumatic diseases. Nat Rev Rheumatol. 2009;5:218–24.CrossRef
3.
go back to reference Brink M, Hansson M, Mathsson L, Jakobsson PJ, Holmdahl R, Hallmans G, et al. Multiplex analyses of antibodies against citrullinated peptides in individuals prior to development of rheumatoid arthritis. Arthritis Rheum. 2013;65:899–910.CrossRef Brink M, Hansson M, Mathsson L, Jakobsson PJ, Holmdahl R, Hallmans G, et al. Multiplex analyses of antibodies against citrullinated peptides in individuals prior to development of rheumatoid arthritis. Arthritis Rheum. 2013;65:899–910.CrossRef
4.
go back to reference 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.CrossRef 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.CrossRef
5.
go back to reference Eke PI, Dye BA, Wei L, Slade GD, Thornton-Evans GO, Borgnakke WS, et al. Update on prevalence of periodontitis in adults in the United States: NHANES 2009 to 2012. J Periodontol. 2015;86:611–22.CrossRef Eke PI, Dye BA, Wei L, Slade GD, Thornton-Evans GO, Borgnakke WS, et al. Update on prevalence of periodontitis in adults in the United States: NHANES 2009 to 2012. J Periodontol. 2015;86:611–22.CrossRef
6.
go back to reference Carasol M, Llodra JC, Fernandez-Meseguer A, Bravo M, Garcia-Margallo MT, Calvo-Bonacho E, et al. Periodontal conditions among employed adults in Spain. J Clin Periodontol. 2016;43:548–56.CrossRef Carasol M, Llodra JC, Fernandez-Meseguer A, Bravo M, Garcia-Margallo MT, Calvo-Bonacho E, et al. Periodontal conditions among employed adults in Spain. J Clin Periodontol. 2016;43:548–56.CrossRef
7.
go back to reference Tonetti MS, Van Dyke TE. Periodontitis and atherosclerotic cardiovascular disease: consensus report of the Joint EFP/AAP Workshop on Periodontitis and Systemic Diseases. J Clin Periodontol. 2013;40 Suppl 14:S24–9.PubMed Tonetti MS, Van Dyke TE. Periodontitis and atherosclerotic cardiovascular disease: consensus report of the Joint EFP/AAP Workshop on Periodontitis and Systemic Diseases. J Clin Periodontol. 2013;40 Suppl 14:S24–9.PubMed
8.
go back to reference Taylor JJ, Preshaw PM, Lalla E. A review of the evidence for pathogenic mechanisms that may link periodontitis and diabetes. J Periodontol. 2013;84:S113–34.CrossRef Taylor JJ, Preshaw PM, Lalla E. A review of the evidence for pathogenic mechanisms that may link periodontitis and diabetes. J Periodontol. 2013;84:S113–34.CrossRef
9.
go back to reference 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.CrossRef 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.CrossRef
10.
go back to reference 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.PubMed 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.PubMed
11.
go back to reference Demmer RT, Molitor JA, Jacobs DR Jr, Michalowicz BS. Periodontal disease, tooth loss and incident rheumatoid arthritis: results from the First National Health and Nutrition Examination Survey and its epidemiological follow-up study. J Clin Periodontol. 2011;38:998–1006.CrossRef Demmer RT, Molitor JA, Jacobs DR Jr, Michalowicz BS. Periodontal disease, tooth loss and incident rheumatoid arthritis: results from the First National Health and Nutrition Examination Survey and its epidemiological follow-up study. J Clin Periodontol. 2011;38:998–1006.CrossRef
12.
go back to reference 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.CrossRef 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.CrossRef
13.
go back to reference 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.CrossRef 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.CrossRef
14.
go back to reference 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;82:1424–32.CrossRef 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;82:1424–32.CrossRef
15.
go back to reference de Pablo P, Dietrich T, Chapple IL, Milward M, Chowdhury M, Charles PJ, et al. The autoantibody repertoire in periodontitis: a role in the induction of autoimmunity to citrullinated proteins in rheumatoid arthritis? Ann Rheum Dis. 2014;73:580–6.CrossRef de Pablo P, Dietrich T, Chapple IL, Milward M, Chowdhury M, Charles PJ, et al. The autoantibody repertoire in periodontitis: a role in the induction of autoimmunity to citrullinated proteins in rheumatoid arthritis? Ann Rheum Dis. 2014;73:580–6.CrossRef
16.
go back to reference 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.CrossRef 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.CrossRef
17.
go back to reference Aletaha D, Neogi T, Silman AJ, Funovits J, Felson DT, Bingham CO 3rd, et al. Rheumatoid arthritis classification criteria: an American College of Rheumatology/European League Against Rheumatism collaborative initiative. Arthritis Rheum. 2010. 2010;62:2569–81. Aletaha D, Neogi T, Silman AJ, Funovits J, Felson DT, Bingham CO 3rd, et al. Rheumatoid arthritis classification criteria: an American College of Rheumatology/European League Against Rheumatism collaborative initiative. Arthritis Rheum. 2010. 2010;62:2569–81.
18.
go back to reference Herrera D, Sanz M, Jepsen S, Needleman I, Roldan S. A systematic review on the effect of systemic antimicrobials as an adjunct to scaling and root planing in periodontitis patients. J Clin Periodontol. 2002;29(Suppl 3):136–59.CrossRef Herrera D, Sanz M, Jepsen S, Needleman I, Roldan S. A systematic review on the effect of systemic antimicrobials as an adjunct to scaling and root planing in periodontitis patients. J Clin Periodontol. 2002;29(Suppl 3):136–59.CrossRef
19.
go back to reference Mavrogiannis M, Ellis JS, Thomason JM, Seymour RA. The management of drug-induced gingival overgrowth. J Clin Periodontol. 2006;33:434–9.CrossRef Mavrogiannis M, Ellis JS, Thomason JM, Seymour RA. The management of drug-induced gingival overgrowth. J Clin Periodontol. 2006;33:434–9.CrossRef
20.
go back to reference 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.CrossRef 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.CrossRef
21.
go back to reference Smolen JS, Breedveld FC, Schiff MH, Kalden JR, Emery P, Eberl G, et al. A simplified disease activity index for rheumatoid arthritis for use in clinical practice. Rheumatology (Oxford). 2003;42:244–57.CrossRef Smolen JS, Breedveld FC, Schiff MH, Kalden JR, Emery P, Eberl G, et al. A simplified disease activity index for rheumatoid arthritis for use in clinical practice. Rheumatology (Oxford). 2003;42:244–57.CrossRef
22.
go back to reference Aletaha D, Nell VP, Stamm T, Uffmann M, Pflugbeil S, Machold K, et al. Acute phase reactants add little to composite disease activity indices for rheumatoid arthritis: validation of a clinical activity score. Arthritis Res Ther. 2005;7:R796–806.CrossRef Aletaha D, Nell VP, Stamm T, Uffmann M, Pflugbeil S, Machold K, et al. Acute phase reactants add little to composite disease activity indices for rheumatoid arthritis: validation of a clinical activity score. Arthritis Res Ther. 2005;7:R796–806.CrossRef
23.
go back to reference Pincus T, Swearingen C, Wolfe F. Toward a multidimensional Health Assessment Questionnaire (MDHAQ): assessment of advanced activities of daily living and psychological status in the patient-friendly health assessment questionnaire format. Arthritis Rheum. 1999;42:2220–30.CrossRef Pincus T, Swearingen C, Wolfe F. Toward a multidimensional Health Assessment Questionnaire (MDHAQ): assessment of advanced activities of daily living and psychological status in the patient-friendly health assessment questionnaire format. Arthritis Rheum. 1999;42:2220–30.CrossRef
24.
go back to reference Silness J, Loe H. Periodontal disease in pregnancy. II. Correlation between oral hygiene and periodontal condtion. Acta Odontol Scand. 1964;22:121–35.CrossRef Silness J, Loe H. Periodontal disease in pregnancy. II. Correlation between oral hygiene and periodontal condtion. Acta Odontol Scand. 1964;22:121–35.CrossRef
25.
go back to reference Ainamo J, Bay I. Problems and proposals for recording gingivitis and plaque. Int Dent J. 1975;25:229–35.PubMed Ainamo J, Bay I. Problems and proposals for recording gingivitis and plaque. Int Dent J. 1975;25:229–35.PubMed
26.
go back to reference Tonetti MS, Claffey N. Advances in the progression of periodontitis and proposal of definitions of a periodontitis case and disease progression for use in risk factor research. Group C consensus report of the 5th European Workshop in Periodontology. J Clin Periodontol. 2005;32(Suppl 6):210–3.CrossRef Tonetti MS, Claffey N. Advances in the progression of periodontitis and proposal of definitions of a periodontitis case and disease progression for use in risk factor research. Group C consensus report of the 5th European Workshop in Periodontology. J Clin Periodontol. 2005;32(Suppl 6):210–3.CrossRef
27.
go back to reference Cohen S, Kamarck T, Mermelstein R. A global measure of perceived stress. J Health Soc Behav. 1983;24:385–96.CrossRef Cohen S, Kamarck T, Mermelstein R. A global measure of perceived stress. J Health Soc Behav. 1983;24:385–96.CrossRef
28.
go back to reference Remor E. Psychometric properties of a European Spanish version of the Perceived Stress Scale (PSS). Span J Psychol. 2006;9:86–93.CrossRef Remor E. Psychometric properties of a European Spanish version of the Perceived Stress Scale (PSS). Span J Psychol. 2006;9:86–93.CrossRef
29.
go back to reference Graffar M. Une méthode de classification social d’ échantillons de population. Courier. 1956;6:455–9. Graffar M. Une méthode de classification social d’ échantillons de population. Courier. 1956;6:455–9.
30.
31.
go back to reference Helminen-Pakkala E, Laine V. The relationship between periodontal findings and articular involvement in a group of subjects suffering from rheumatoid arthritis. Proc Finn Dent Soc. 1973;69:52–5.PubMed Helminen-Pakkala E, Laine V. The relationship between periodontal findings and articular involvement in a group of subjects suffering from rheumatoid arthritis. Proc Finn Dent Soc. 1973;69:52–5.PubMed
32.
go back to reference Sjostrom L, Laurell L, Hugoson A, Hakansson JP. Periodontal conditions in adults with rheumatoid arthritis. Community Dent Oral Epidemiol. 1989;17:234–6.CrossRef Sjostrom L, Laurell L, Hugoson A, Hakansson JP. Periodontal conditions in adults with rheumatoid arthritis. Community Dent Oral Epidemiol. 1989;17:234–6.CrossRef
33.
go back to reference Yavuzyilmaz E, Yamalik N, Calguner M, Ersoy F, Baykara M, Yeniay I. Clinical and immunological characteristics of patients with rheumatoid arthritis and periodontal disease. J Nihon Univ Sch Dent. 1992;34:89–95.CrossRef Yavuzyilmaz E, Yamalik N, Calguner M, Ersoy F, Baykara M, Yeniay I. Clinical and immunological characteristics of patients with rheumatoid arthritis and periodontal disease. J Nihon Univ Sch Dent. 1992;34:89–95.CrossRef
34.
go back to reference Joseph R, Rajappan S, Nath SG, Paul BJ. Association between chronic periodontitis and rheumatoid arthritis: a hospital-based case-control study. Rheumatol Int. 2013;33:103–9.CrossRef Joseph R, Rajappan S, Nath SG, Paul BJ. Association between chronic periodontitis and rheumatoid arthritis: a hospital-based case-control study. Rheumatol Int. 2013;33:103–9.CrossRef
35.
go back to reference Mercado FB, Marshall RI, Klestov AC, Bartold PM. Relationship between rheumatoid arthritis and periodontitis. J Periodontol. 2001;72:779–87.CrossRef Mercado FB, Marshall RI, Klestov AC, Bartold PM. Relationship between rheumatoid arthritis and periodontitis. J Periodontol. 2001;72:779–87.CrossRef
36.
go back to reference Pischon N, Pischon T, Kroger J, Gulmez E, Kleber BM, Bernimoulin JP, et al. Association among rheumatoid arthritis, oral hygiene, and periodontitis. J Periodontol. 2008;79:979–86.CrossRef Pischon N, Pischon T, Kroger J, Gulmez E, Kleber BM, Bernimoulin JP, et al. Association among rheumatoid arthritis, oral hygiene, and periodontitis. J Periodontol. 2008;79:979–86.CrossRef
37.
go back to reference Potempa J, Mydel P, Koziel J. The case for periodontitis in the pathogenesis of rheumatoid arthritis. Nat Rev Rheumatol. 2017;13:606–20.CrossRef Potempa J, Mydel P, Koziel J. The case for periodontitis in the pathogenesis of rheumatoid arthritis. Nat Rev Rheumatol. 2017;13:606–20.CrossRef
38.
go back to reference Mobini M, Maboudi A, Ali Mohammadpour R. Periodontitis in rheumatoid arthritis patients, abundance and association with disease activity. Med J Islam Repub Iran. 2017;31:44.CrossRef Mobini M, Maboudi A, Ali Mohammadpour R. Periodontitis in rheumatoid arthritis patients, abundance and association with disease activity. Med J Islam Repub Iran. 2017;31:44.CrossRef
39.
go back to reference Ayravainen L, Leirisalo-Repo M, Kuuliala A, Ahola K, Koivuniemi R, Meurman JH, et al. Periodontitis in early and chronic rheumatoid arthritis: a prospective follow-up study in Finnish population. BMJ Open. 2017;7:e011916.CrossRef Ayravainen L, Leirisalo-Repo M, Kuuliala A, Ahola K, Koivuniemi R, Meurman JH, et al. Periodontitis in early and chronic rheumatoid arthritis: a prospective follow-up study in Finnish population. BMJ Open. 2017;7:e011916.CrossRef
40.
go back to reference 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.CrossRef 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.CrossRef
41.
go back to reference Kobayashi T, Okada M, Ito S, Kobayashi D, Ishida K, Kojima A, et al. Assessment of interleukin-6 receptor inhibition therapy on periodontal condition in patients with rheumatoid arthritis and chronic periodontitis. J Periodontol. 2014;85:57–67.CrossRef Kobayashi T, Okada M, Ito S, Kobayashi D, Ishida K, Kojima A, et al. Assessment of interleukin-6 receptor inhibition therapy on periodontal condition in patients with rheumatoid arthritis and chronic periodontitis. J Periodontol. 2014;85:57–67.CrossRef
42.
go back to reference Coat J, Demoersman J, Beuzit S, Cornec D, Devauchelle-Pensec V, Saraux A, et al. Anti-B lymphocyte immunotherapy is associated with improvement of periodontal status in subjects with rheumatoid arthritis. J Clin Periodontol. 2015;42:817–23.CrossRef Coat J, Demoersman J, Beuzit S, Cornec D, Devauchelle-Pensec V, Saraux A, et al. Anti-B lymphocyte immunotherapy is associated with improvement of periodontal status in subjects with rheumatoid arthritis. J Clin Periodontol. 2015;42:817–23.CrossRef
43.
go back to reference 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.CrossRef 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.CrossRef
44.
go back to reference 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.CrossRef 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.CrossRef
45.
go back to reference Kobayashi T, Yokoyama T, Ito S, Kobayashi D, Yamagata A, Okada M, et al. Periodontal and serum protein profiles in patients with rheumatoid arthritis treated with tumor necrosis factor inhibitor adalimumab. J Periodontol. 2014;85:1480–8.CrossRef Kobayashi T, Yokoyama T, Ito S, Kobayashi D, Yamagata A, Okada M, et al. Periodontal and serum protein profiles in patients with rheumatoid arthritis treated with tumor necrosis factor inhibitor adalimumab. J Periodontol. 2014;85:1480–8.CrossRef
46.
go back to reference Ziebolz D, Rupprecht A, Schmickler J, Bothmann L, Kramer J, Patschan D, et al. Association of different immunosuppressive medications with periodontal condition in patients with rheumatoid arthritis: results from a cross-sectional study. J Periodontol. 2018;89:1310–7.CrossRef Ziebolz D, Rupprecht A, Schmickler J, Bothmann L, Kramer J, Patschan D, et al. Association of different immunosuppressive medications with periodontal condition in patients with rheumatoid arthritis: results from a cross-sectional study. J Periodontol. 2018;89:1310–7.CrossRef
47.
go back to reference Gonzalez SM, Payne JB, Yu F, Thiele GM, Erickson AR, Johnson PG, et al. Alveolar bone loss is associated with circulating anti-citrullinated protein antibody (ACPA) in patients with rheumatoid arthritis. J Periodontol. 2015;86:222–31.CrossRef Gonzalez SM, Payne JB, Yu F, Thiele GM, Erickson AR, Johnson PG, et al. Alveolar bone loss is associated with circulating anti-citrullinated protein antibody (ACPA) in patients with rheumatoid arthritis. J Periodontol. 2015;86:222–31.CrossRef
48.
go back to reference Goh CE, Kopp J, Papapanou PN, Molitor JA, Demmer RT. Association between serum antibodies to periodontal bacteria and rheumatoid factor in the Third National Health and Nutrition Examination Survey. Arthritis Rheumatol. 2016;68:2384–93.CrossRef Goh CE, Kopp J, Papapanou PN, Molitor JA, Demmer RT. Association between serum antibodies to periodontal bacteria and rheumatoid factor in the Third National Health and Nutrition Examination Survey. Arthritis Rheumatol. 2016;68:2384–93.CrossRef
49.
go back to reference Lee JY, Choi IA, Kim JH, Kim KH, Lee EY, Lee EB, et al. 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. 2015;16:190.CrossRef Lee JY, Choi IA, Kim JH, Kim KH, Lee EY, Lee EB, et al. 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. 2015;16:190.CrossRef
50.
go back to reference 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.CrossRef 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.CrossRef
51.
go back to reference Matuliene G, Pjetursson BE, Salvi GE, Schmidlin K, Bragger U, Zwahlen M, et al. Influence of residual pockets on progression of periodontitis and tooth loss: results after 11 years of maintenance. J Clin Periodontol. 2008;35:685–95.CrossRef Matuliene G, Pjetursson BE, Salvi GE, Schmidlin K, Bragger U, Zwahlen M, et al. Influence of residual pockets on progression of periodontitis and tooth loss: results after 11 years of maintenance. J Clin Periodontol. 2008;35:685–95.CrossRef
52.
go back to reference Schatzle M, Faddy MJ, Cullinan MP, Seymour GJ, Lang NP, Burgin W, et al. The clinical course of chronic periodontitis: V. Predictive factors in periodontal disease. J Clin Periodontol. 2009;36:365–71.CrossRef Schatzle M, Faddy MJ, Cullinan MP, Seymour GJ, Lang NP, Burgin W, et al. The clinical course of chronic periodontitis: V. Predictive factors in periodontal disease. J Clin Periodontol. 2009;36:365–71.CrossRef
53.
go back to reference Van der Velden U, Abbas F, Armand S, Loos BG, Timmerman MF, Van der Weijden GA, et al. Java project on periodontal diseases. The natural development of periodontitis: risk factors, risk predictors and risk determinants. J Clin Periodontol. 2006;33:540–8.CrossRef Van der Velden U, Abbas F, Armand S, Loos BG, Timmerman MF, Van der Weijden GA, et al. Java project on periodontal diseases. The natural development of periodontitis: risk factors, risk predictors and risk determinants. J Clin Periodontol. 2006;33:540–8.CrossRef
54.
go back to reference Akinkugbe AA, Saraiya VM, Preisser JS, Offenbacher S, Beck JD. Bias in estimating the cross-sectional smoking, alcohol, obesity and diabetes associations with moderate-severe periodontitis in the Atherosclerosis Risk in Communities study: comparison of full versus partial-mouth estimates. J Clin Periodontol. 2015;42:609–21.CrossRef Akinkugbe AA, Saraiya VM, Preisser JS, Offenbacher S, Beck JD. Bias in estimating the cross-sectional smoking, alcohol, obesity and diabetes associations with moderate-severe periodontitis in the Atherosclerosis Risk in Communities study: comparison of full versus partial-mouth estimates. J Clin Periodontol. 2015;42:609–21.CrossRef
Metadata
Title
Association between severity of periodontitis and clinical activity in rheumatoid arthritis patients: a case–control study
Authors
Beatriz Rodríguez-Lozano
Jerián González-Febles
Jorge Luis Garnier-Rodríguez
Shashi Dadlani
Sagrario Bustabad-Reyes
Mariano Sanz
Fernando Sánchez-Alonso
Carlos Sánchez-Piedra
Enrique González-Dávila
Federico Díaz-González
Publication date
01-12-2019
Publisher
BioMed Central
Published in
Arthritis Research & Therapy / Issue 1/2019
Electronic ISSN: 1478-6362
DOI
https://doi.org/10.1186/s13075-019-1808-z

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