Browse > Article
http://dx.doi.org/10.5051/jpis.2018.48.6.347

Periodontal pathogens and the association between periodontitis and rheumatoid arthritis in Korean adults  

Kim, Jin-Hee (Department of Periodontology, Seoul National University School of Dentistry)
Choi, In Ah (Department of Internal Medicine, Chungbuk National University Hospital)
Lee, Joo Youn (Department of Molecular Medicine and Biopharmaceutical Sciences, Seoul National University)
Kim, Kyoung-Hwa (Department of Periodontology, Seoul National University School of Dentistry)
Kim, Sungtae (Department of Periodontology, Seoul National University School of Dentistry)
Koo, Ki-Tae (Department of Periodontology, Seoul National University School of Dentistry)
Kim, Tae-Il (Department of Periodontology, Seoul National University School of Dentistry)
Seol, Yang-Jo (Department of Periodontology, Seoul National University School of Dentistry)
Ku, Young (Department of Periodontology, Seoul National University School of Dentistry)
Rhyu, In-Chul (Department of Periodontology, Seoul National University School of Dentistry)
Song, Yeong Wook (Department of Molecular Medicine and Biopharmaceutical Sciences, Seoul National University)
Lee, Yong-Moo (Department of Periodontology, Seoul National University School of Dentistry)
Publication Information
Journal of Periodontal and Implant Science / v.48, no.6, 2018 , pp. 347-359 More about this Journal
Abstract
Purpose: Periodontitis and rheumatoid arthritis (RA) share a similar inflammatory pathogenesis. Porphyromonas gingivalis (Pg) can induce anticyclic-citrullinated peptide autoantibodies (anti-CCP antibodies), a key factor in the development of RA. This study aimed at evaluating the relationships between the 2 diseases and identifying the clinical implications thereof, with a focus on periodontal pathogens in Korean adults. Methods: A total of 260 RA patients and 86 age- and sex-matched control patients without arthritis were enrolled in this prospective cross-sectional study. Periodontal indices and the prevalence and amount of periodontal pathogens were compared between the groups. Correlations between periodontal and RA indices were examined, as were correlations between 9 periodontal pathogens and RA indices. Results: The RA group had significantly higher values than the control group for all investigated periodontal indices (P<0.05) except the number of teeth. The gingival index (GI) was correlated with the disease activity score 28 (DAS28) (r=0.125, P=0.049), RA disease duration (r=0.253, P<0.001), erythrocyte sedimentation rate (ESR) (r=0.162, P=0.010), and anti-CCP antibody titer (r=0.205, P=0.004). Probing pocket depth (PPD) was correlated with ESR (r=0.139, P=0.027) and anti-Pg antibody titer (r=0.203, P=0.001). Bleeding on probing (BOP) was correlated with DAS28 (r=0.137, P=0.030), RA disease duration (r=0.202, P=0.001), ESR (r=0.136, P=0.030), anti-Pg antibody titer (r=0.177, P=0.005), and anti-CCP antibody titer (r=0.188, P=0.007). Clinical attachment level (CAL) and periodontitis severity were correlated with anti-Pg antibody titer (the former r=0.201, P=0.002; the latter r=0.175, P=0.006). The quantity of Pg was positively correlated with the serum anti-Pg antibody titer (r=0.148, P=0.020). Conclusions: The GI, BOP, and PPD showed positive relationships with several RA indices. The anti-Pg antibody titer had positive relationships with PPD, BOP, CAL, and periodontitis severity. Thus, increasing values of periodontal indices could be used as a risk indicator of disease development in RA patients, and an increasing anti-Pg antibody titer could be considered as a warning sign in RA patients suffering with periodontitis.
Keywords
Anti-Pg titer; Periodontitis; Porphyromonas gingivalis; Rheumatoid arthritis;
Citations & Related Records
Times Cited By KSCI : 1  (Citation Analysis)
연도 인용수 순위
1 Page RC, Kornman KS. The pathogenesis of human periodontitis: an introduction. Periodontol 2000 1997;14:9-11.   DOI
2 Armitage GC, Research S; Research, Science and Therapy Committee of the American Academy of Periodontology. Diagnosis of periodontal diseases. J Periodontol 2003;74:1237-47.   DOI
3 Mercado FB, Marshall RI, Bartold PM. Inter-relationships between rheumatoid arthritis and periodontal disease. A review. J Clin Periodontol 2003;30:761-72.   DOI
4 Rutger Persson G. Rheumatoid arthritis and periodontitis - inflammatory and infectious connections. Review of the literature. J Oral Microbiol 2012;4:4.
5 Kaur S, White S, Bartold PM. Periodontal disease and rheumatoid arthritis: a systematic review. J Dent Res 2013;92:399-408.   DOI
6 Golub LM, Payne JB, Reinhardt RA, Nieman G. Can systemic diseases co-induce (not just exacerbate) periodontitis? A hypothetical "two-hit" model. J Dent Res 2006;85:102-5.   DOI
7 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.   DOI
8 Martinez-Martinez RE, Abud-Mendoza C, Patino-Marin N, Rizo-Rodriguez JC, Little JW, Loyola-Rodriguez JP. Detection of periodontal bacterial DNA in serum and synovial fluid in refractory rheumatoid arthritis patients. J Clin Periodontol 2009;36:1004-10.   DOI
9 McGraw WT, Potempa J, Farley D, Travis J. Purification, characterization, and sequence analysis of a potential virulence factor from Porphyromonas gingivalis, peptidylarginine deiminase. Infect Immun 1999;67:3248-56.
10 Bartold PM, Marshall RI, Haynes DR. Periodontitis and rheumatoid arthritis: a review. J Periodontol 2005;76:2066-74.   DOI
11 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.   DOI
12 Schmickler J, Rupprecht A, Patschan S, Patschan D, Muller GA, Haak R, et al. Cross-sectional evaluation of periodontal status and microbiologic and rheumatoid parameters in a large cohort of patients with rheumatoid arthritis. J Periodontol 2017;88:368-79.   DOI
13 Choi IA, Kim JH, Kim YM, Lee JY, Kim KH, Lee EY, et al. Periodontitis is associated with rheumatoid arthritis: a study with longstanding rheumatoid arthritis patients in Korea. Korean J Intern Med 2016;31:977-86.   DOI
14 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.   DOI
15 Armitage GC. Development of a classification system for periodontal diseases and conditions. Ann Periodontol 1999;4:1-6.   DOI
16 Vander Cruyssen B, Van Looy S, Wyns B, Westhovens R, Durez P, Van den Bosch F, et al. DAS28 best reflects the physician's clinical judgment of response to infliximab therapy in rheumatoid arthritis patients: validation of the DAS28 score in patients under infliximab treatment. Arthritis Res Ther 2005;7:R1063-71.   DOI
17 Silness J, Loe H. Periodontal disease in pregnancy. Ii. Correlation between oral hygiene and periodontal condtion. Acta Odontol Scand 1964;22:121-35.   DOI
18 Loe H, Silness J. Periodontal disease in pregnancy. I. Prevalence and severity. Acta Odontol Scand 1963;21:533-51.   DOI
19 Socransky SS, Haffajee AD, Cugini MA, Smith C, Kent RL Jr. Microbial complexes in subgingival plaque. J Clin Periodontol 1998;25:134-44.   DOI
20 Papapanou PN. Periodontal diseases: epidemiology. Ann Periodontol 1996;1:1-36.   DOI
21 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.   DOI
22 Mirrielees J, Crofford LJ, Lin Y, Kryscio RJ, Dawson DR 3rd, Ebersole JL, et al. Rheumatoid arthritis and salivary biomarkers of periodontal disease. J Clin Periodontol 2010;37:1068-74.   DOI
23 Garib BT, Qaradaxi SS. Temporomandibular joint problems and periodontal condition in rheumatoid arthritis patients in relation to their rheumatologic status. J Oral Maxillofac Surg 2011;69:2971-8.   DOI
24 Biyikoglu B, Buduneli N, Kardesler 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.   DOI
25 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.   DOI
26 Harvey GP, Fitzsimmons TR, Dhamarpatni AA, Marchant C, Haynes DR, Bartold PM. Expression of peptidylarginine deiminase-2 and -4, citrullinated proteins and anti-citrullinated protein antibodies in human gingiva. J Periodontal Res 2013;48:252-61.   DOI
27 Bozkurt FY, Yetkin Ay Z, Berker E, Tepe E, Akkus S. Anti-inflammatory cytokines in gingival crevicular fluid in patients with periodontitis and rheumatoid arthritis: a preliminary report. Cytokine 2006;35:180-5.   DOI
28 Ishi EP, Bertolo MB, Rossa C Jr, Kirkwood KL, Onofre MA. Periodontal condition in patients with rheumatoid arthritis. Braz Oral Res 2008;22:72-7.   DOI
29 Gleissner C, Willershausen B, Kaesser U, Bolten WW. The role of risk factors for periodontal disease in patients with rheumatoid arthritis. Eur J Med Res 1998;3:387-92.
30 Kasser UR, Gleissner C, Dehne F, Michel A, Willershausen-Zonnchen B, Bolten WW. Risk for periodontal disease in patients with longstanding rheumatoid arthritis. Arthritis Rheum 1997;40:2248-51.   DOI
31 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.   DOI
32 Naito Y, Okuda K, Takazoe I, Watanabe H, Ishikawa I. The relationship between serum IgG levels to subgingival gram-negative bacteria and degree of periodontal destruction. J Dent Res 1985;64:1306-10.   DOI
33 Konig MF, Abusleme L, Reinholdt J, Palmer RJ, Teles RP, Sampson K, et al. Aggregatibacter actinomycetemcomitans-induced hypercitrullination links periodontal infection to autoimmunity in rheumatoid arthritis. Sci Transl Med 2016;8:369ra176.   DOI
34 Mikuls TR, Payne JB, Reinhardt RA, Thiele GM, Maziarz E, Cannella AC, et al. Antibody responses to Porphyromonas gingivalis (P. gingivalis) in subjects with rheumatoid arthritis and periodontitis. Int Immunopharmacol 2009;9:38-42.   DOI
35 Hitchon CA, Chandad F, Ferucci ED, Willemze A, Ioan-Facsinay A, van der Woude D, et al. Antibodies to porphyromonas gingivalis are associated with anticitrullinated protein antibodies in patients with rheumatoid arthritis and their relatives. J Rheumatol 2010;37:1105-12.   DOI
36 Lamster IB, Kaluszhner-Shapira I, Herrera-Abreu M, Sinha R, Grbic JT. Serum IgG antibody response to Actinobacillus actinomycetemcomitans and Porphyromonas gingivalis: implications for periodontal diagnosis. J Clin Periodontol 1998;25:510-6.   DOI
37 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.   DOI
38 Heliovaara M, Aho K, Aromaa A, Knekt P, Reunanen A. Smoking and risk of rheumatoid arthritis. J Rheumatol 1993;20:1830-5.
39 Silman AJ, Newman J, MacGregor AJ. Cigarette smoking increases the risk of rheumatoid arthritis. Results from a nationwide study of disease-discordant twins. Arthritis Rheum 1996;39:732-5.   DOI
40 Dougados M, Soubrier M, Antunez A, Balint P, Balsa A, Buch MH, et al. Prevalence of comorbidities in rheumatoid arthritis and evaluation of their monitoring: results of an international, cross-sectional study (COMORA). Ann Rheum Dis 2014;73:62-8.