References

rsp

Научно-практическая ревматология

Rheumatology Science and Practice

1995-44841995-4492

IMA-PRESS, LLC

10.14412/1995-4484-2018-613-621

rsp-2626

Research Article

ПРОГРЕСС В РЕВМАТОЛОГИИ В XXI ВЕКЕ

PROGRESS IN RHEUMATOLOGY IN THE XXI CENTURY

Пародонтит – предвестник ревматоидного артрита?

IS PERIODONTITIS A HARBINGER OF RHEUMATOID ARTHRITIS?

Гордеев

А. В.

Gordeev

A. V.

профессор, зав. лабораторией ранних артритов, докт. мед. наук

115522, Москва, Каширское шоссе, 34А

34A, Kashirskoe Shosse, Moscow 115522

avg1305@yandex.ru

Галушко

Е. А.

Galushko

E. A.

ведущий научный сотрудник лаборатории ранних артритов, докт. мед. наук

115522, Москва, Каширское шоссе, 34А

34A, Kashirskoe Shosse, Moscow 115522

Савушкина

Н. М.

Savushkina

N. M.

младший научный сотрудник лаборатории ранних артритов, канд. мед. наук

115522, Москва, Каширское шоссе, 34А

34A, Kashirskoe Shosse, Moscow 115522

Лила

А. М.

Lila

A. M.

профессор, директор ФГБНУ НИИР им. В.А. Насоновой, докт. мед. наук

115522, Москва, Каширское шоссе, 34А

34A, Kashirskoe Shosse, Moscow 115522

ФГБНУ «Научно-исследовательский институт ревматологии им. В.А. Насоновой»РоссияV.A. Nasonova Research Institute of RheumatologyRussian Federation

2018

08112018

565613621

2018

Гордеев А.В., Галушко Е.А., Савушкина Н.М., Лила А.М.

Gordeev A.V., Galushko E.A., Savushkina N.M., Lila A.M.

Данная работа распространяется под лицензией Creative Commons Attribution 4.0.

This work is licensed under a Creative Commons Attribution 4.0 License.

https://rsp.mediar-press.net/rsp/article/view/2626

В настоящее время в ревматологии все большее внимание уделяется выявлению заболеваний на максимально ранних сроках (преклинических стадиях), что может способствовать более благоприятному ответу на терапию. С этой целью в качестве возможных предикторов их развития изучаются различные клинические, лабораторные (в первую очередь, иммунологические) и инструментальные показатели. В качестве одного из возможных факторов развития ревматических болезней, в частности ревматоидного артрита (РА), могут выступать заболевания пародонта (ЗП). В настоящем обзоре рассмотрены вопросы взаимосвязи между развитием пародонтита и РА, обсуждается участие отдельных микроорганизмов в патогенезе ЗП и РА. Обозначены клеточно-опосредованные механизмы, вызывающие хронический воспалительный процесс и приводящие к резорбции костей. Описана роль ЗП и P. gingivalis в процессах нарушения цитруллинирования аутоантигенов. Рассмотрена возможность использования генно-инженерных биологических препаратов для лечения ревматических заболеваний, сопровождающихся наличием тяжелых форм ЗП.

Increasing attention in rheumatology is currently paid to the detection of diseases in the earliest (preclinical) stages, which can contribute to a more favorable response to therapy. To this end, various clinical, laboratory (and primarily immunological) and instrumental parameters are studied as a possible harbinger of rheumatic diseases (RDs). Periodontal diseases (PD) may be possible predictors for the development of RDs, and particularly rheumatoid arthritis (RA). This review considers the relationship between the development of periodontitis and RA and discusses the participation of individual microorganisms in the pathogenesis of PD and RA. The cell-mediated mechanisms that cause the chronic inflammatory process and lead to bone resorption are discussed. The role of PD and P. gingivalis in the processes of impaired autoantigen citrullination is described. Whether biological agents may be used to treat RDs accompanied by severe PD is considered.

ревматоидный артритпародонтитзаболевания

rheumatoid arthritisperiodontitisdiseases

References1

Насонов ЕЛ, Лила АМ, Галушко ЕА, Амирджанова ВН. Стратегия развития ревматологии: от научных достижений к практическому здравоохранению. Научно-практическая ревматология. 2017;55(4):339-43 [Nasonov EL, Lila AM, Galushko EA, Amirdzhanova VN. Strategy for development of rheumatology: From scientific achievements to practical healthcare. Nauchno-Prakticheskaya Revmatologiya = Rheumatology Science and Practice. 2017;55(4):339-43 (In Russ.)]. doi: 10.14412/1995-4484-2017-339-343.

Насонов ЕЛ. Применение генно-инженерных биологических препаратов для лечения ревматоидного артрита: общая характеристика. В кн.: Насонов ЕЛ, редактор. Генно-инженерные биологические препараты в лечении ревматоидного артрита. Москва: ИМА-ПРЕСС; 2013. С. 123-37 [Nasonov EL. Application of genetically engineered biological drugs for the treatment of rheumatoid arthritis. In: Nasonov EL, editor. Genno-inzhenernye biologicheskie preparaty v lechenii revmatoidnogo artrita [Genetically engineered biological drugs in the treatment of rheumatoid arthritis]. Moscow: IMA-PRESS; 2013. P. 123-37 (In Russ.)].

Smolen JS, Landewe R, Breedveld FC, et al. EULAR recommendations for the management of rheumatoid arthritis with synthetic and biological disease-modifying antirheumatic drugs: 2013 update. Ann Rheum Dis. 2014;73:492-509. doi: 10.1136/annrheumdis-2013-204573

Насонов ЕЛ. Проблемы иммунопатологии ревматоидного артрита: эволюция болезни. Научно-практическая ревматология. 2017;55(3):277-94 [Nasonov EL. Problems of rheumatoid arthritis immunopathology: Evolution of the disease. Nauchno-Prakticheskaya Revmatologiya = Rheumatology Science and Practice. 2017;55(3):277-94 (In Russ.)]. doi: 10.14412/1995-4484-2017-277-294

Галушко ЕА, Гордеев АВ. Концепция «болезни барьерного органа» в патогенезе спондилоартритов. Научно-практическая ревматология. 2016;54(2):199-205 [Galushko EA, Gordeev AV. The concept of barrier organ disease in the pathogenesis of spondyloarthritis. Nauchno-Prakticheskaya Revmatologiya = Rheumatology Science and Practice. 2016;54(2):199-205 (In Russ.)]. doi: 10.14412/1995-4484-2016-199-205

The Human Microbiome Project Consortium. Structure, function and diversity of the healthy human microbiome. Nature. 2012;486:207-14. doi: 10.1038/nature11234

Pischon N, Pischon T, Krü ger J, et al. Association among rheumatoid arthritis, oral hygiene, and periodontitis. J Periodontol. 2008 Jun;79(6):979-86. doi: 10.1902/jop.2008.070501

Wade WG. The oral microbiome in health and disease. Pharmacol Res. 2013;69:137-43. doi: 10.1016/j.phrs.2012.11.006

Anonymous. American academy of periodontology task force report on the update to the 1999 classification of periodontal diseases and conditions. J Periodontol. 2015;86(7):835-8. doi: 10.1902/jop.2015.157001

Helenius LM, Meurman JH, Helenius I, et al. Oral and salivary parameters in patients with rheumatic diseases. Acta Odontol Scand. 2005 Oct;63(5):284-93. doi: 10.1080/00016350510020043

Craig RG, Boylan R, Yip J, et al. Serum IgG antibody response to periodontal pathogens in minority populations: relationship to periodontal disease status and progression. J Periodontal Res. 2002;37:132-46. doi: 10.1034/j.1600-0765.2002.00031.x

Ouedraogo DD, Tiendrebeogo J, Guiguimde PL, et al. Periodontal disease in patients with rheumatoid arthritis in Sub-Saharan Africa: A case-control study. Joint Bone Spine. 2017 Jan;84(1):113-4. doi: 10.1016/j.jbspin.2016.02.014. Epub 2016 Mar 17.

Havemose-Poulsen A, Sorensen LK, Stoltze K, et al. Cytokine profiles in peripheral blood and whole blood cell cultures associated with aggressive periodontitis, juvenile idiopathic arthritis, and rheumatoid arthritis. J Periodontol. 2005 Dec;76(12):2276-85. doi: 10.1902/jop.2005.76.12.2276

De Pablo P, Dietrich T, McAlindon TE. Association of periodontal disease and tooth loss with rheumatoid arthritis in the US population. J Rheumatol. 2008 Jan;35(1):70-6. Epub 2007 Nov 15.

Chen HH, Huang N, Chen YM, et al. Association between a history of periodontitis and the risk of rheumatoid arthritis: a nationwide, population-based, casecontrol study. Ann Rheum Dis. 2013;72:1206-11. doi: 10.1136/annrheumdis-2012-201593

Mercado FB, Marshall RI, Klestov AC. Relationship between rheumatoid arthritis and periodontitis. J Periodontol. 2001;72:779-87. doi: 10.1902/jop.2001.72.6.779

Marotte H, Farge P, Gaudin P, et al. The association between periodontal disease and joint destraction in rheumatoid arthritis extends the link between the HLA-DR shared epitope and severity of bone destraction. Ann Rheum Dis. 2006;65:905-9. doi: 10.1136/ard.2005.036913

Stein J, Reichert S, Gautsch A, et al. Are there HLA combinations typical supporting for or making resistant against aggressive and/or chronic periodontitis? J Periodontal Res. 2003;38:508-17. doi: 10.1034/j.1600-0765.2003.00683.x

Dewhirst FE, Chen T, Izard J, et al. The human oral microbiome. J Bacteriol. 2010;192:5002-17. doi: 10.1128/JB.00542-10

Smolik I, Robinson D, El-Gabalawy HS. Periodontitis and rheumatoid arthritis: epidemiologic, clinical, and immunologic associations. Compend Contin Educ Dent. 2009 May;30(4):188-90, 192, 194 passim; quiz 198, 210.

Van Winkelhoff AJ, Loos BG, van der Reijden WA, et al. Porphyromonas gingivalis, Bacteroides forsythus and other putative periodontal pathogens in subjects with and without periodontal destruction. J Clin Periodontol. 2002;29:1023-8.doi: 10.1034/j.1600-051X.2002.291107.x

Rams TE, Listgarten MA, Slots J. Utility of 5 major putative periodontal pathogens and selected clinical parameters to predict periodontal breakdown on maintenance care. J Clin Peridontol. 1996;23:346-54. doi: 10.1111/j.1600-051X.1996.tb00556.x

Moen K, Brun JG, Madland TM, et al. Immunoglobulin G and A antibody responses to Bacteroides forsythus and Prevotella intermedia in sera and synovial fluids of arthritis patients. Clin Diagn Lab Immunol. 2003;10:1043-50.

Rams TE, Listgarten MA, Slots J. Actinobacillus actinomycetemcomitans and Porphyromonas gingivalis subgingival presence, species-specific serum immunoglobulin G antibody levels, and periodontitis disease recurrence. J Peridontal Res. 2006;41:228-34. doi: 10.1111/j.1600-0765.2005.00860.x

Furuichi Y, Shimotsu A, Ito H, et al. Associations of periodontal status with general health conditions and serum antibody titers for Porphyromonas gingivalis and Actinobacillus actinomycetemcomitans. J Periodontol. 2003;74:1491-7. doi: 10.1902/jop.2003.74.10.1491

Van Winkelhoff AJ, Bosch-Tijhof CJ, Winkel EG, et al. Smoking affects the subgingival microflora in periodontitis. J Periodontol. 2001;72:666-71. doi: 10.1902/jop.2001.72.5.666

Contreras A, Umeda M, Chen C, et al. Relationship between herpes viruses and adult periodontitis and periodontopathic bacteria. J Periodontol 1999;70:478-84. doi: 10.1902/jop.1999.70.5.478

Slots J, Kamma JJ, Sugar C. The herpes virus – Porphyromonas gingivalis periodontitis axis. J Periodontal Res. 2003;38:318-23. doi: 10.1034/j.1600-0765.2003.00659.x

Kubar A, Saygun I, Ozdemir A, et al. Real-time polymerase chain reaction quantification of human cytomegalovirus and Epstein- Barr virus in periodontal pockets and the adjacent gingiva of periodontitis lesions. J Periodontal Res. 2005;40:97-104. doi: 10.1111/j.1600-0765.2005.00770.x

Martinez-Martinez RE, Abud-Mendoza C, Patino-Marin N, et al. Detection of periodontal bacterial DNA in serum and synovial fluid in refractory rheumatoid arthritis patients. J Clin Periodontol. 2009;36:1004-10. doi: 10.1111/j.1600-051X.2009.01496.x

Moen K, Brun JG, Valen M, et al. Synovial inflammation in active rheumatoid arthritis and psoriatic arthritis facilitates trapping of a variety of oral bacterial DNAs. Clin Exp Rheumatol. 2006;24:656-63.

Berglundh T, Donati M. Aspects of adaptive host response in periodontitis. J Clin Periodontol. 2005;32 Suppl. 6:87-107. doi: 10.1111/j.1600-051X.2005.00820.x

Gamonal J, Acevedo A, Bascones A, et al. Levels of interleukin-1 beta, -8, and -10 and RANTES in gingival crevicular fluid and cell populations in adult periodontitis patients and the effect of periodontal treatment. J Periodontol. 2000;71:1535-45. doi: 10.1902/jop.2000.71.10.1535

Cutler CW, Jotwani R, Palucka KA, et al. Evidence and a novel hypothesis for the role of dendritic cells and Porphyromonas gingivalis in adult periodontitis. J Periodontal Res. 1999;34:406-12. doi: 10.1111/j.1600-0765.1999.tb02274.x

Nakajima T, Ueki-Maruyama K, Oda T, et al. Regulatory T-cells infiltrate periodontal disease tissues. J Dent Res. 2005;84:639-43. doi: 10.1177/154405910508400711

Zitzmann NU, Berglundh T, Lindhe J. Inflammatory lesions in the gingiva following resective/non-resective periodontal therapy. J Clin Periodontol. 2005;32:139-46. doi: 10.1111/j.1600-051X.2005.00649.x

Moshref M, Mashhadi-Abbass F, Sargolzaei S, et al. Extramedullary plasmocytoma of the gingiva. Arch Iran Med. 2007;10:91-3.

Kinane DF, Lappin DF, Koulouri O, et al. Humoral immune responses in periodontal disease may have mucosal and systemic immune features. Clin Exp Immunol. 1999;115:534-41. doi: 10.1046/j.1365-2249.1999.00819.x

Nakajima T, Amanuma R, Ueki-Maruyama J, et al. CXCL13 expression and follicular dendritic cells in relation to B-cell infiltration in periodontal disease tissues. J Periodontal Res. 2008;43:635-41. doi: 10.1111/j.1600-0765.2008.01042.x

Harada Y, Han X, Yamashita K, et al. Effect of adoptive transfer of antigen-specific B cells on periodontal bone resorption. J Periodontal Res. 2006;41:101-7. doi: 10.1111/j.1600-0765.2005.00839.x

Gemmell E, Carter CL, Hart DN, et al. Antigen-presenting cells in human periodontal disease tissues. Oral Microbiol Immunol. 2002;17:388-93. doi: 10.1034/j.1399-302X.2002.170609.x

Berglundh T, Donati M, Zitzmann N. B cells in periodontitis: friends or enemies? Periodontology. 2007;45:51-66. doi: 10.1111/j.1600-0757.2007.00223.x

Faizuddin M, Bharathi SH, Rohini NV. Estimation of interleukin-1beta levels in the gingival crevicular fluid in health and in inflammatory periodontal disease. J Periodontal Res. 2003;38:111-4. doi: 10.1034/j.1600-0765.2003.01649.x

Biyikoglu B, Buduneli N, Kardesler L, et al. Evaluation of t-PA, PAI-2, IL-1beta and pgE(2) in gingival crevicular fluid of rheumatoid arthritis patients with periodontal disease. J Clin Periodontol. 2006;33:605-11. doi: 10.1111/j.1600-051X.2006.00961.x

Kobayashi T, Ito S, Kuroda T, et al. The interleukin-1 and Fcgamma receptor gene polymorphisms in Japanese patients with rheumatoid arthritis and periodontitis. J Periodontol. 2007;78:2311-8. doi: 10.1902/jop.2007.070136

Vernal R, Dutzan N, Chaparro A, et al. Levels of interleukin-17 in gingival crevicular fluid and in supernatants of cellular cultures of gingival tissue from patients with chronic periodontitis. J Clin Periodontol. 2005;32:383-9. doi: 10.1111/j.1600-051X.2005.00684.x

Yu JJ, Ruddy MJ, Wong GC, et al. An essential role for IL-17 in preventing pathogen-initiated bone destruction: recruitment of neutrophils to inflamed bone requires IL-17 receptor-dependent signals. Blood. 2007;109:3794-802. doi: 10.1182/blood-2005-09-010116

Bostanci N, Ilgenli T, Emingil G, et al. Gingival crevicular fluid levels of RANKL and OPG in periodontal diseases: implications of their relative ratio. J Clin Periodontol. 2007;34:367-9. doi: 10.1111/j.1600-051X.2007.01061.x

Kawai T, Matsuyama T, Hosokawa Y, et al. B and T lymphocytes are the primary sources of RANKL in the bone resorptive lesion of periodontal disease. Am J Pathol. 2006;169:987-98. doi: 10.2353/ajpath.2006.060180

Lu HK, Chen YL, Chang HC, et al. Identification of the osteoprotegerin/ receptor activator of nuclear factor-kappa B ligand system in gingival crevicular fluid and tissue of patients with chronic periodontitis. J Peridontol Res. 2006;41:354-60. doi: 10.1111/j.1600-0765.2006.00883.x

Bostanci N, Ilgenli T, Emingil G, et al. Differential expression of receptor activator of nuclear factor-kappa B ligand and osteoprotegerin mRNA in periodontal diseases. J Periodontol Res. 2007;42:287-93. doi: 10.1111/j.1600-0765.2006.00946.x

Taubman MA, Valverde P, Han X, et al. Immune response: the key to bone resorption in periodontal disease. J Periodontol. 2005;76 Suppl. 11:2033-41. doi: 10.1902/jop.2005.76.11-S.2033

Han X, Kawai T, Eastcott JW, et al. Bacterial-responsive B lymphocytes induce periodontal bone resorption. J Immunol. 2006;176:625-31. doi: 10.4049/jimmunol.176.1.625

Colucci S, Mori G, Brunetti G, et al. Interleukin-7 production by B lymphocytes affects the T cell-dependent osteoclast formation in an in vitro model derived from human periodontitis patients. Int J Immunopathol Pharmacol. 2005;18 Suppl. 3:13-9.

Wara-aswapati N, Surarit R, Chayasadom A, et al. RANKL upregulation associated with periodontitis and Porphyromonas gingivalis. J Periodontol. 2007;78:1062-9. doi: 10.1902/jop.2007.060398

Belibasakis GN, Bostanci N, Hashim A, et al. Regulation of RANKL and OPG gene expression in human gingival fibroblasts and periodontal ligament cells by Porphyromonas gingivalis: a putative role of the Arg-gingipains. Microb Pathog. 2007;43:46-53. doi: 10.1016/j.micpath.2007.03.001

Vis M, Havaardsholm EA, Haugeberg G, et al. Evaluation of bonemineral density, bone metabolism, osteoprotegerin and receptor activator of the NFkappaB ligand serum levels during treatment with infliximab in patients with rheumatoid arthritis. Ann Rheum Dis. 2006;65:1495-9. doi: 10.1136/ard.2005.044198

Pers JO, Saraux A, Pierre R, et al. 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. doi: 10.1902/jop.2008.070616

Garlet GP, Cardoso CR, Silva TA, et al. Cytokine pattern determines the progression of experimental periodontal disease induced by Actinobacillus actinomycetemcomitans through the modulation of MMPs, RANKL, and their physiological inhibitors. Oral Microbiol Immunol. 2006;21:12-20. doi: 10.1111/j.1399-302X.2005.00245.x

Rosenstein ED, Greenwald RA, Kushner LJ, et al. Hypothesis: the humoral immune response to oral bacteria provides a stimulus for the development of rheumatoid arthritis. Inflammation. 2004;28:311-8. doi: 10.1007/s10753-004-6641-z

Hamevose-Poulsen A, Westergaard J, Stoltze K, et al. Periodontal and hematological characteristics associated with aggressive periodontitis, juvenile idiopathic arthritis, and rheumatoid arthritis. J Periodontol. 2006;77:280-8. doi: 10.1902/jop.2006.050051

Molitor JA, Alonso A, Wener MH, et al. Moderate to severe adult periodontitis increases risk of rheumatoid arthritis in non-smokers and is associated with elevated ACPA titers: the ARIC study. Arthritis Rheum. 2009;60 Suppl. 10:S433.

Mikuls TR, Thiele GM, Deane KD, et al. Porphyromonas gingivalis and Disease-Related Autoantibodies in Individuals at Increased Risk of Rheumatoid Arthritis. Arthritis Rheum. 2012 Nov;64(11):3522-30. doi: 10.1002/art.34595

Nesse W, Westra J, van der Wal JE, et al. The periodontium contains citrullinated proteins, PAD-2 enzymes and HC Gp-39. Arthritis Rheum. 2009;60(Suppl.10):S434-5.

Soory M. Periodontal diseases and rheumatoid arthritis: a coincident model for therapeutic intervention? Curr Drug Metab. 2007;8:750-7. doi: 10.2174/138920007782798162

Berthelot JM, Le Goff B, Maugars Y. Thymic Hassall's corpuscles, regulatory Tcells, and rheumatoid arthritis. Semin Arthritis Rheum. 2010;39:347-55. doi: 10.1016/j.semarthrit.2008.08.010

Seror R, Gall-David S, Bonnaure-Mallet M. Association of Anti-Porphyromonas gingivalis Antibody Titers With Nonsmoking Status in Early Rheumatoid Arthritis. Arthritis Rheum. 2015;67(7):1729-37. doi: 10.1002/art.39118

Arvikar SL, Collier DS, Fisher MC, et al. Clinical correlations with Porphyromonas gingivalis antibody responses in patients with early rheumatoid arthritis. Arthritis Res Ther. 2013;15:R109. doi: 10.1186/ar4289

Pers JO, d'Arbonneau F, Devauchelle-Pensec V, et al. Is periodontal disease mediated by salivary BAFF in Sjö gren's syndrome? Arthritis Rheum. 2005 Aug;52(8):2411-4. doi: 10.1002/art.21205

Kuru B, McCullough MJ, Yilmaz S, Porter SR. Clinical and microbiological studies of periodontal disease in Sjö gren syndrome patients. J Clin Periodontol. 2002 Feb;29(2):92-102. doi: 10.1034/j.1600-051x.2002.290202.x

Ortiz P, Bissada NF, Palomo L, 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: 10.1902/jop.2009.080447

Mayer Y, Balbir-Gurman A, Machtei EE. Anti-tumor necrosis factor-alpha therapy and periodontal parameters in patients with rheumatoid arthritis. J Periodontol. 2009 Sep;80:1414-20. doi: 10.1902/jop.2009.090015

Coat J, Demoersman J, Beuzit S, 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. doi: 10.1111/jcpe.12433

Kobayashi T, Okada M, Ito S, 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. doi: 10.1902/jop.2013.120696

The authors declare that there are no conflicts of interest present.