Correlation between rheumatoid arthritis and periodontitis

Authors

DOI:

https://doi.org/10.15584/ejcem.2022.4.11

Keywords:

Aggregatibacter actinomycetemcomitans, periodontitis, Porphyromonas gingivalis, rheumatoid arthritis, risk factors

Abstract

Introduction and aim. The association between periodontitis (PD) and rheumatoid arthritis (RA) has been analyzed and described in literature. Periodontal pathogens, such as Porphyromonas gingivalis and Aggregatibacter actinomycetemcomitans are pointed as the common factors for both diseases. In this work we demonstrate that treatment of dental and oral diseases is an unconditional requirement for patients with RA.

Material and methods. PubMed was searched with the keyword “rheumatoid arthritis” and “periodontitis” from May 1999 to January 2022, showed 181 articles. Ultimately 72 articles were included in the review.

Analysis of the literature. The above mentioned pathogens exhibit multiple mechanisms that disturb immune and inflammatory responses of the human organism. Those mechanisms lead to the periodontal disease (PD) that may activate the systematic reactions which in turn lead to intensification of systematic diseases such as rheumatoid arthritis (RA). P. gingivalis has the ability to expresses PAD enzyme (peptidylarginine deiminase) and activates the citrullization process. Moreover, the bacterium produces gingipain cysteine proteinases, which degrade the mechanisms of immunological system. The latter pathogen, A. actinomycetemcomitans, expresses hypercitrullization in neutrophils.

Conclusion. Both pathogens influence inflammatory response of the organism, through the common pro-inflammatory mediators for periodontitis and rheumatoid arthritis, intensify the clinical manifestations of both diseases.

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References

Renvert S, Berglund JS, Persson GR, Söderlin MK. The association between rheumatoid arthritis and periodontal disease in a population-based cross-sectional case-control study. BMC Rheumatol. 2020;4:31. doi: 10.1186/s41927-020-00129-4

Varshney S, Sharma M, Kapoor S, Siddharth M. Association between rheumatoid arthritis and periodontitis in an adult population – A cross sectional study. J Clin Exp Dent. 2021;13:10. doi: 10.4317/jced.57562

Moura MF, Cota LOM, Costa AM, Silva TA, Costa FO. Rheumatoid arthritis associated with the occurance, severity and extension of periodontitis: A case control study. J Clin Exp Dent. 2021;13(4):e389-e396. doi: 10.4317/jced.57540

De Luca F, Shoenfeld Y. The microbiome in autoimmune diseases. Clin Exp Immunol. 2019;195(1):74-85. doi: 10.1111/cei.13158

Ceccarelli F, Saccucci M, Di Carlo G, et al. Periodontitis and Rheumatoid Arthritis: The Same Inflammatory Mediators? Mediators Inflamm. 2019;2019:6034546. doi: 10.1155/2019/6034546

Mei F, Xie M, Huang X, et al. Porphyromonas gingivalis and Its Systemic Impact: Current Status. Pathogens. 2020; 9(11):944. doi: 10.3390/pathogens9110944

Darrah E, Andrade F. Rheumatoid arthritis and citrullination. Curr Opin Rheumatol. 2018;30(1):72-78. doi: 10.1097/bor.0000000000000452

Ding N, Luo M, Wen YH, Li RY, Bao QY. The Effects of Non-Surgical Periodontitis Therapy on the Clinical Features and Serological Parameters of Patients Suffering from Rheumatoid Arthritis as Well as Chronic Periodontitis. J Inflamm Res. 2022;15:177-185. doi: 10.2147/jir.s326896

Guo Q, Wang Y, Xu D, Nossent J, Pavlos NJ, Xu J. Rheumatoid arthritis: pathological mechanisms and modern pharmacologic therapies. Bone Res. 2018;6:15. doi: 10.1038/s41413-018-0016-9

Smolen JS, Aletaha D, McInnes IB. Rheumatoid arthritis. Lancet. 2016;388(10055):2023-2038. doi: 10.1016/s0140-6736(16)30173-8

Pihlstrom BL, Michalowicz BS, Johnson NW. Periodontal diseases. Lancet. 2005;366(9499):1809-1820. doi: 10.1016/s0140-6736(05)67728-8

Kwon T, Lamster IB, Levin L. Current Concepts in the Management of Periodontitis. Int Dent J. 2021;71(6):462-476. doi: 10.1111/idj.12630

Kinane DF, Stathopoulou PG, Papapanou PN. Periodontal diseases. Nat Rev Dis Primers. 2017;3:17038. doi: 10.1038/nrdp.2017.38

How KY, Song KP, Chan KG. Porphyromonas gingivalis: An Overview of Periodontopathic Pathogen below the Gum Line. Front Microbiol. 2016;7:53. doi: 10.3389/fmicb.2016.00053

Kumar PS. From focal sepsis to periodontal medicine: a century of exploring the role of the oral microbiome in systemic disease. J Physiol. 2017;595(2):465-476. doi:10.1113/jp272427

Rahajoe PS, Smit MJ, Kertia N, Westra J, Vissink A. Cytokines in gingivocrevicular fluid of rheumatoid arthritis patients: A review of the literature. Oral Dis. 2019;25(6):1423-1434. doi: 10.1111/odi.13145

Gabarrini G, Grasso S, van Winkelhoff A, van Dijl J. Gingimaps: Protein Localization in the Oral Pathogen Porphyromonas gingivalis. Review. Microbiol Mol Biol Rev. 2020;84(1):e00032-19. doi: 10.1128/MMBR.00032-19

Bostanci N, Belibasakis GN. Porphyromonas gingivalis: an invasive and evasive opportunistic oral pathogen. FEMS Microbiol Lett. 2012;333(1):1-9. doi: 10.1111/j.1574-6968.2012.02579.x

Schmidt J, Jentsch H, Stingu CS, Sack U. General immune status and oral microbiology in patients with different forms of periodontitis and healthy control subjects. PLoS One. 2014;9(10):e109187. doi: 10.1371/journal.pone.0109187

Rovas A, Puriene A, Punceviciene E, Butrimiene I, Stuopelyte K, Jarmalaite S. Associations of periodontal statis in periodontitis and rheumatorid arthritis patients. J Periodontal Implant Sci. 2021;51;2.

Liao F, Li Z, Wang Y, Shi B, Gong Z, Cheng X. Porphyromonas gingivalis may play an important role in the pathogenesis of periodontitis-associated rheumatoid arthritis. Med Hypotheses. 2009;72(6):732-735. doi: 10.1016/j.mehy.2008.12.040

Gabarrini G, de Smit M, Westra J, et al. The peptidylarginine deiminase gene is a conserved feature of Porphyromonas gingivalis. Sci Rep. 2015;5:13936. doi: 10.1038/srep13936

Gómez-Bañuelos E, Mukherjee A, Darrah E, Andrade F. Rheumatoid Arthritis-Associated Mechanisms of Porphyromonas gingivalis and Aggregatibacter actinomycetemcomitans. J Clin Med. 2019;8(9):1309. doi: 10.3390/jcm8091309

Mikuls TR, Payne JB, Reinhardt RA, et al. Antibody responses to Porphyromonas gingivalis (P. gingivalis) in subjects with rheumatoid arthritis and periodontitis. Int Immunopharmacol. 2009;9(1):38-42. doi: 10.1016/j.intimp.2008.09.008

Mikuls TR, Payne JB, Yu F, et al. Periodontitis and Porphyromonas gingivalis in patients with rheumatoid arthritis. Arthritis Rheumatol. 2014;66(5):1090-100. doi: 10.1002/art.38348

Makrygiannakis D, af Klint E, Lundberg IE, et al. Citrullination is an inflammation-dependent process. Ann Rheum Dis. 2006;65(9):1219-1222. doi: 10.1136/ard.2005.049403

Snir O, Widhe M, Hermansson M, et al. Antibodies to several citrullinated antigens are enriched in the joints of rheumatoid arthritis patients. Arthritis Rheum. 2010;62(1):44-52. doi: 10.1002/art.25036

Kinloch A, Lundberg K, Wait R, et al. Synovial fluid is a site of citrullination of autoantigens in inflammatory arthritis. Arthritis Rheum. 2008;58(8):2287-2295. doi: 10.1002/art.23618

Fuggle NR, Smith TO, Kaul A, Sofat N. Hand to Mouth: A Systematic Review and Meta-Analysis of the Association between Rheumatoid Arthritis and Periodontitis. Front Immunol. 2016;7:80. doi:10.3389/fimmu.2016.00080

Wegner N, Wait R, Sroka A, et al. Peptidylarginine deiminase from Porphyromonas gingivalis citrullinates human fibrinogen and α-enolase: implications for autoimmunity in rheumatoid arthritis. Arthritis Rheum. 2010;62(9):2662-2672. doi: 10.1002/art.27552

de Smit M, Westra J, Vissink A, Doornbos-van der Meer B, Brouwer E, van Winkelhoff AJ. Periodontitis in established rheumatoid arthritis patients: a cross-sectional clinical, microbiological and serological study. Arthritis Res Ther. 2012;14(5):R222. doi: 10.1186/ar4061

Stathopoulou PG, Benakanakere MR, Galicia JC, Kinane DF. The host cytokine response to Porphyromonas gingivalis is modified by gingipains. Oral Microbiol Immunol. 2009;24(1):11-17. doi: 10.1111/j.1399-302X.2008.00467.x

Hajishengallis G. Immunomicrobial pathogenesis of periodontitis: keystones, pathobionts, and host response. Trends Immunol. 2014;35(1):3-11. doi: 10.1016/j.it.2013.09.001

Moutsopoulos NM, Kling HM, Angelov N, et al. Porphyromonas gingivalis promotes Th17 inducing pathways in chronic periodontitis. J Autoimmun. 2012;39(4):294-303. doi: 10.1016/j.jaut.2012.03.003

Jauregui CE, Wang Q, Wright CJ, Takeuchi H, Uriarte SM, Lamont RJ. Suppression of T-cell chemokines by Porphyromonas gingivalis. Infect Immun. 2013;81(7):2288-2295. doi: 10.1128/iai.00264-13

Gaddis DE, Maynard CL, Weaver CT, Michalek SM, Katz J. Role of TLR2-dependent IL-10 production in the inhibition of the initial IFN-γ T cell response to Porphyromonas gingivalis. J Leukoc Biol. 2013;93(1):21-31. doi: 10.1189/jlb.0512220

Firestein GS, McInnes IB. Immunopathogenesis of Rheumatoid Arthritis. Immunity. 2017;46(2):183-196. doi: 10.1016/j.immuni.2017.02.006

Hajishengallis G, Abe T, Maekawa T, Hajishengallis E, Lambris JD. Role of complement in host-microbe homeostasis of the periodontium. Semin Immunol. 2013;25(1):65-72. doi: 10.1016/j.smim.2013.04.004

Potempa J, Pike RN. Corruption of innate immunity by bacterial proteases. J Innate Immun. 2009;1(2):70-87. doi: 10.1159/000181144

Slaney JM, Gallagher A, Aduse-Opoku J, Pell K, Curtis MA. Mechanisms of resistance of Porphyromonas gingivalis to killing by serum complement. Infect Immun. 2006;74(9):5352-5361. doi: 10.1128/iai.00304-06

Hajishengallis G, Lamont RJ. Breaking bad: manipulation of the host response by Porphyromonas gingivalis. Eur J Immunol. 2014;44(2):328-338. doi: 10.1002/eji.201344202

Krauss JL, Potempa J, Lambris JD, Hajishengallis G. Complementary Tolls in the periodontium: how periodontal bacteria modify complement and Toll-like receptor responses to prevail in the host. Periodontol. 2010;52(1):141-162. doi: 10.1111/j.1600-0757.2009.00324.x

Maekawa T, Krauss JL, Abe T, et al. Porphyromonas gingivalis manipulates complement and TLR signaling to uncouple bacterial clearance from inflammation and promote dysbiosis. Cell Host & Microbe. 2014;15:6.

Hajishengallis G. Periodontitis: from microbial immune subversion to systemic inflammation. Nat Rev Immunol. 2015;15(1):30-44. doi: 10.1038/nri3785

Jia L, Han N, Du J, Guo L, Luo Z, Liu Y. Pathogenesis of Important Virulence Factors of Porphyromonas gingivalis via Toll-Like Receptors. Front Cell Infect Microbiol. 2019;9:262. doi: 10.3389/fcimb.2019.00262

Mysak J, Podzimek S, Sommerova P, et al. Porphyromonas gingivalis: Major Periodontopathic Pathogen Overview. J Immunol Res. 2014;2014:476068. doi: 10.1155/2014/476068

Wang M, Krauss JL, Domon H, et al. Microbial hijacking of complement-toll-like receptor crosstalk. Sci Signal. 2010;3(109):ra11. doi:10.1126/scisignal.2000697

Abe T, Hosur KB, Hajishengallis E, et al. Local complement-targeted intervention in periodontitis: proof-of-concept using a C5a receptor (CD88) antagonist. J Immunol. 2012;189(11):5442-5448. doi: 10.4049/jimmunol.1202339

Curtis MA, Percival RS, Devine D, et al. Temperature-dependent modulation of Porphyromonas gingivalis lipid A structure and interaction with the innate host defenses. Infect Immun. 2011;79(3):1187-1193. doi:10.1128/iai.00900-10

Zenobia C, Hajishengallis G. Basic biology and role of interleukin-17 in immunity and inflammation. Periodontol. 2015;69(1):142-159. doi: 10.1111/prd.12083

Shaker OG, Ghallab NA. IL-17 and IL-11 GCF levels in aggressive and chronic periodontitis patients: relation to PCR bacterial detection. Mediators Inflamm. 2012;2012:174764. doi: 10.1155/2012/174764

Cheng WC, van Asten SD, Burns LA, et al. Periodontitis-associated pathogens P. gingivalis and A. actinomycetemcomitans activate human CD14(+) monocytes leading to enhanced Th17/IL-17 responses. Eur J Immunol. 2016;46(9):2211-2221. doi: 10.1002/eji.201545871

Behfarnia P, Birang R, Pishva SS, Hakemi MG, Khorasani MM. Expression levels of th-2 and th-17 characteristic genes in healthy tissue versus periodontitis. J Dent (Tehran). 2013;10(1):23-31.

Chabaud M, Lubberts E, Joosten L, van Den Berg W, Miossec P. IL-17 derived from juxta-articular bone and synovium contributes to joint degradation in rheumatoid arthritis. Arthritis Res. 2001;3(3):168-177. doi: 10.1186/ar294

Kotake S, Udagawa N, Takahashi N, et al. IL-17 in synovial fluids from patients with rheumatoid arthritis is a potent stimulator of osteoclastogenesis. J Clin Invest. 1999;103(9):1345-1352. doi: 10.1172/jci5703

Di Benedetto A, Gigante I, Colucci S, Grano M. Periodontal disease: linking the primary inflammation to bone loss. Clin Dev Immunol. 2013;2013:503754. doi: 10.1155/2013/503754

Graves D. Cytokines that promote periodontal tissue destruction. J Periodontol. 2008;79(8):1585-1591. doi:10.1902/jop.2008.080183

Kato Y, Hagiwara M, Ishihara Y, et al. TNF-α augmented Porphyromonas gingivalis invasion in human gingival epithelial cells through Rab5 and ICAM-1. BMC Microbiol. 2014;14:229. doi: 10.1186/s12866-014-0229-z

Palm E, Khalaf H, Bengtsson T. Porphyromonas gingivalis downregulates the immune response of fibroblasts. BMC Microbiol. 2013;13:155. doi: 10.1186/1471-2180-13-155

Tanaka T, Narazaki M, Kishimoto T. IL-6 in inflammation, immunity, and disease. Cold Spring Harb Perspect Biol. 2014;6(10):a016295. doi: 10.1101/cshperspect.a016295

Pan W, Wang Q, Chen Q. The cytokine network involved in the host immune response to periodontitis. Int J Oral Sci. 2019;11(3):30. doi: 10.1038/s41368-019-0064-z

Srirangan S, Choy EH. The role of interleukin 6 in the pathophysiology of rheumatoid arthritis. Ther Adv Musculoskelet Dis. 2010;2(5):247-56. doi: 10.1177/1759720x10378372

Naruishi K, Nagata T. Biological effects of interleukin-6 on Gingival Fibroblasts: Cytokine regulation in periodontitis. J Cell Physiol. 2018;233(9):6393-6400. doi:10.1002/jcp.26521

Herath TD, Wang Y, Seneviratne CJ, et al. Porphyromonas gingivalis lipopolysaccharide lipid A heterogeneity differentially modulates the expression of IL-6 and IL-8 in human gingival fibroblasts. J Clin Periodontol. 2011;38(8):694-701. doi: 10.1111/j.1600-051X.2011.01741.x

Ridwan RD, Sidarningsih, Kusumaningsih T, Salim S. Effect of lipopolysaccharide derived from surabaya isolates of Actinobacillus actinomycetemcomitans on alveolar bone destruction. Vet World. 2018;11(2):161-166. doi: 10.14202/vetworld.2018.161-166

Pahumunto N, Ruangsri P, Wongsuwanlert M, Piwat S, Dahlen G, Teanpaisan R. Aggregatibacter actinomycetemcomitans serotypes and DGGE subtypes in Thai adults with chronic periodontitis. Arch Oral Biol. 2015;60(12):1789-1796. doi: 10.1016/j.archoralbio.2015.09.003

Konig MF, Abusleme L, Reinholdt J, et al. Aggregatibacter actinomycetemcomitans-induced hypercitrullination links periodontal infection to autoimmunity in rheumatoid arthritis. Sci Transl Med. 2016;8(369):369ra176. doi: 10.1126/scitranslmed.aaj1921

Derksen V, Huizinga TWJ, van der Woude D. The role of autoantibodies in the pathophysiology of rheumatoid arthritis. Semin Immunopathol. 2017;39(4):437-446. doi: 10.1007/s00281-017-0627-z

Kelk P, Claesson R, Chen C, Sjöstedt A, Johansson A. IL-1beta secretion induced by Aggregatibacter (Actinobacillus) actinomycetemcomitans is mainly caused by the leukotoxin. Int J Med Microbiol. 2008;298(5-6):529-541. doi: 10.1016/j.ijmm.2007.06.005

Dinarello CA. Interleukin-1 in the pathogenesis and treatment of inflammatory diseases. Blood. 2011;117(14):3720-3732. doi: 10.1182/blood-2010-07-273417

Barksby HE, Lea SR, Preshaw PM, Taylor JJ. The expanding family of interleukin-1 cytokines and their role in destructive inflammatory disorders. Clin Exp Immunol. 2007;149(2):217-225. doi: 10.1111/j.1365-2249.2007.03441.x

Caielli S, Banchereau J, Pascual V. Neutrophils come of age in chronic inflammation. Curr Opin Immunol. 2012;24(6):671-677. doi: 10.1016/j.coi.2012.09.008

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2022-12-30

How to Cite

Zielińska, A., & Tabarkiewicz, J. (2022). Correlation between rheumatoid arthritis and periodontitis. European Journal of Clinical and Experimental Medicine, 20(4), 451–458. https://doi.org/10.15584/ejcem.2022.4.11

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