Emre AVCI, Gülbahar USTAOĞLU, Murat TAŞÇI, Duygu GÖLLER BULUT, Deniz YAMAN

Dental and temporomandibular joint alterations in rheumatoid arthritis patients and their association with salivary oxidative stress

Background/aim: Rheumatoid arthritis (RA) is the most extensive inflammatory arthritis causing permanent deformities in the joint. Increasing evidence suggests that oxidative stress is a substantial factor in the pathogenesis of RA. This study aimed to examine the salivary oxidant-antioxidant status of RA and control groups and to compare these biomarkers by correlating them with disease activity, acute phase reactants, and clinical findings. Materials and methods: Age and sex-matched 60 participants including 30 patients with RA and 30 control (50 females, 10 males; mean age: 42.62 ± 10.89 years) were evaluated. RA disease activity and severity were evaluated by the disease activity score 28-C reactive protein (DAS 28-CRP). Rheumatoid factor (RF) positivity, anticitrullinated protein antibodies (ACPA) positivity, erythrocyte sedimentation rate (ESR), CRP, tender and swollen joint counts, and medical treatment regimens of the patients (glucocorticoids, conventional or biologic disease-modifying antirheumatic drugs) were recorded. In the radiographic examination, dental findings, and bone alterations of the temporomandibular joint (TMJ) were recorded and compared for both groups. Saliva samples were obtained for analysis of total antioxidant status (TAS), total oxidant status (TOS), arylesterase (ARE), and oxidative stress index (OSI) levels. The data analysis was conducted by independent sample t-test and chi-square test. Results: Condylar erosion was the most common radiographic change in TMJ of RA patients. Osteophyte formation was a prominent finding in the control group. Lower TAS and higher OSI levels were found in RA patients compared with controls (p = 0.013; p = 0.029, respectively). The effect of DAS 28-CRP score on the levels of oxidative stress biomarkers in RA patients was not significant. Conclusion: Oxidative stress causes tissue damage in response to excessive mechanical loading, which in turn promotes TMD. However, disease activity has not a prominent impact on the salivary oxidative stress status of RA patients.Key words: Oxidative stress, rheumatoid arthritis, saliva, temporomandibular joint disorders

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1. Cheng Z, Meade J, Mankia K, Emery P, Devine DA. Periodontal disease and periodontal bacteria as triggers for rheumatoid arthritis. Best Practice & Research: Clinical Rheumatology 2017; 31 (1): 19-30. doi: 10.1016/j.berh.2017.08.001
2. Garib BT, Qaradaxi SS. Temporomandibular joint problems and periodontal condition in rheumatoid arthritis patients in relation to their rheumatologic status. Journal of Oral and Maxillofacial Surgery 2011; 69 (12): 2971-2978. doi: 10.1016/j. joms.2011.02.131
3. Yilmaz HH, Yildirim D, Ugan Y, Tunc SE, Yesildag A et al. Clinical and magnetic resonance imaging findings of the temporomandibular joint and masticatory muscles in patients with rheumatoid arthritis. Rheumatology International 2012; 32 (5): 1171-1178. doi: 10.1007/s00296-010-1743-4
4. Ogus H. Rheumatoid arthritis of the temporomandibular joint. British Journal of Oral Surgery 1975; 12 (3): 275-284. doi: 10.1016/0007-117x(75)90058-x
5. Tabeling HJ, Dolwick MF. Rheumatoid arthritis: diagnosis and treatment. Florida Dental Journal 1985; 56 (1): 16-18.
6. Jaswal S, Mehta HC, Sood AK, Kaur J. Antioxidant status in rheumatoid arthritis and role of antioxidant therapy. Clinica Chimica Acta 2003; 338 (1-2): 123-129. doi: 10.1016/j. cccn.2003.08.011
7. Seven A, Güzel S, Aslan M, Hamuryudan V. Lipid, protein, DNA oxidation and antioxidant status in rheumatoid arthritis. Clinical Biochemistry 2008; 41 (7-8): 538-543. doi: 10.1016/j. clinbiochem.2008.01.029
8. Mateen S, Moin S, Khan AQ, Zafar A, Fatima N. Increased reactive oxygen species formation and oxidative stress in rheumatoid arthritis. PloS One 2016; 11 (4): e0152925. doi: 10.1371/journal.pone.0152925
9. Afonso V, Champy R, Mitrovic D, Collin P, Lomri A. Reactive oxygen species and superoxide dismutases: role in joint diseases. Joint Bone Spine 2007; 74 (4): 324-329. doi: 10.1016/j. jbspin.2007.02.002
10. Nagler RM, Klein I, Zarzhevsky N, Drigues N, Reznick AZ. Characterization of the differentiated antioxidant profile of human saliva. Free Radical Biology and Medicine 2002; 32 (3): 268-277. doi: 10.1016/s0891-5849(01)00806-1
11. Ighodaro OM, Akinloye OA. First line defence antioxidantssuperoxide dismutase (SOD), catalase (CAT) and glutathione peroxidase (GPX): their fundamental role in the entire antioxidant defence grid. Alexandria Journal of Medicine 2018; 54 (4): 287-293.
12. Erel O. A new automated colorimetric method for measuring total oxidant status. Clinical Biochemistry 2005; 38 (12): 1103- 1111. doi: 10.1016/j.clinbiochem.2005.08.008
13. Serdar Z, Aslan K, Dirican M, Sarandöl E, Yeşilbursa D et al. Lipid and protein oxidation and antioxidant status in patients with angiographically proven coronary artery disease. Clinical Biochemistry 2006; 39 (8): 794-803. doi: 10.1016/j. clinbiochem.2006.02.004
14. Isik A, Koca SS, Ustundag B, Celik H, Yildirim A. Paraoxonase and arylesterase levels in rheumatoid arthritis. Clinical Rheumatology 2007; 26 (3): 342-348. doi: 10.1007/s10067-006- 0300-8
15. Aletaha D, Neogi T, Silman AJ, Funovits J, Felson DT et al. 2010 rheumatoid arthritis classification criteria: an American College of Rheumatology/European League against rheumatism collaborative initiative. Arthritis & Rheumatism 2010; 62 (9): 2569-2581. doi: 10.1002/art.27584
16. Prevoo MLL, Van’T Hof M, Kuper HH, Van Leeuwen MA, Van De Putte LBA et al. Modified disease activity scores that include twenty-eight-joint counts development and validation in a prospective longitudinal study of patients with rheumatoid arthritis. Arthritis & Rheumatism: Official Journal of the American College of 1995; 38 (1): 44-48. doi: 10.1002/ art.1780380107
17. Truelove E, Pan W, Look JO, Mancl LA, Ohrbach RK et al. The research diagnostic criteria for temporomandibular disorders. III: validity of axis I diagnoses. Journal of Orofacial Pain 2010; 24 (1): 35-47.
18. Steenks MH, De Wijer A. Validity of the research diagnostic criteria for temporomandibular disorders axis I in clinical and research settings. Journal of Orofacial Pain 2009; 23 (1).
19. Wiese M, Svensson P, Bakke M, List T, Hintze H et al. Association between temporomandibular joint symptoms, signs, and clinical diagnosis using the RDC/TMD and radiographic findings in temporomandibular joint tomograms. Journal of Orofacial Pain 2008; 22 (3).
20. Gambhir JK, Lali P, Jain AK. Correlation between blood antioxidant levels and lipid peroxidation in rheumatoid arthritis. Clinical Biochemistry 1997; 30 (4): 351-355. doi: 10.1016/s0009-9120(96)00007-0
21. Yumru M, Savas HA, Kalenderoglu A, Bulut M, Celik H et al. Oxidative imbalance in bipolar disorder subtypes: a comparative study. Progress in Neuro-Psychopharmacology and Biological Psychiatry 2009; 33 (6): 1070-1074. doi: 10.1016/j.pnpbp.2009.06.005
22. Kosecik M, Erel O, Sevinc E, Selek S. Increased oxidative stress in children exposed to passive smoking. International Journal of Cardiology 2005; 100 (1): 61-64. doi: 10.1016/j. ijcard.2004.05.069
23. Kundu S, Ghosh P, Datta S, Ghosh A, Chattopadhyay S et al. Oxidative stress as a potential biomarker for determining disease activity in patients with rheumatoid arthritis. Free Radical Research 2012; 46 (12): 1482-1489. doi: 10.3109/10715762.2012.727991
24. Lin YC, Hsu ML, Yang JS, Liang TH, Chou SL et al. Temporomandibular joint disorders in patients with rheumatoid arthritis. Journal of the Chinese Medical Association 2007; 70 (12): 527-534. doi: 10.1016/S1726- 4901(08)70055-8
25. Tegelberg A, Kopp S. Subjective symptoms from the stomatognathic system in individuals with rheumatoid arthritis and osteoarthrosis. Swedish Dental Journal 1987; 11 (1-2): 11-22.
26. Voog U, Alstergren P, Eliasson S, Leibur E, Kallikorm R et al. Inflammatory mediators and radiographic changes in temporomandibular joints of patients with rheumatoid arthritis. Acta Odontologica Scandinavica 2003; 61 (1): 57-64. doi: 10.1080/ode.61.1.57.64
27. Goupille P, Fouquet B, Cotty P, Goga D, Valat JP. Direct coronal computed tomography of the temporomandibular joint in patients with rheumatoid arthritis. The British Journal of Radiology 1992; 65 (779): 955-960. doi: 10.1259/0007-1285- 65-779-995
28. Cai HX, Luo JM, Long X, Li XD, Cheng Y. Free-radical oxidation and superoxide dismutase activity in synovial fluid of patients with temporomandibular disorders. Journal of Orofacial Pain 2006; 20 (1): 53-58.
29. Grevers G, Späth M, Krüger K, Schattenkirchner M. Immunodiagnostic findings in” secondary” Sjögren syndrome in chronic polyarthritis. Laryngo-Rhino-Otologie 1990; 69 (11): 605-607. doi: 10.1055/s-2007-998262
30. Karincaoglu Y, Batcioglu K, Erdem T, Esrefoglu M, Genc M. The levels of plasma and salivary antioxidants in the patient with recurrent aphthous stomatitis. Journal of Oral Pathology & Medicine 2005; 34 (1): 7-12. doi: 10.1111/j.1600- 0714.2004.00253.x
31. Baskol G, Demir H, Baskol M, Kilic E, Ates F et al. Assessment of paraoxonase 1 activity and malondialdehyde levels in patients with rheumatoid arthritis. Clinical Biochemistry 2005; 38 (10): 951-955. doi: 10.1016/j.clinbiochem.2005.06.010
32. Altındağ Ö, Karakoç M, Soran N, Çelik H, Çelik N et al. Paraoxonase and arylesterase activities in patients with rheumatoid Arthritis. Romatizma/Rheumatism 2007; 22 (4).
33. Rodríguez de Sotillo D, Velly AM, Hadley M, Fricton JR. Evidence of oxidative stress in temporomandibular disorders: a pilot study. Journal of Oral Rehabilitation 2011; 38 (10): 722- 728. doi: 10.1111/j.1365-2842.2011.02216.x
34. de Almeida C, Amenábar JM. Changes in the salivary oxidative status in individuals with temporomandibular disorders and pain. Journal of Oral Biology and Craniofacial Research 2016; 6: S1-S4. doi: 10.1016/j.jobcr.2016.10.006
35. Coaccioli S, Panaccione A, Biondi R, Sabatini C, Landucci P et al. Evaluation of oxidative stress in rheumatoid and psoriatic arthritis and psoriasis. La Clinica Terapeutica 2009; 160 (6): 467-472.
36. Esen Ç, Alkan BA, Kırnap M, Akgül O, Işıkoğlu S et al. The effects of chronic periodontitis and rheumatoid arthritis on serum and gingival crevicular fluid total antioxidant/oxidant status and oxidative stress index. Journal of Periodontology 2012; 83 (6): 773-779. doi: 10.1902/jop.2011.110420
37. De Pablo P, Dietrich T, McAlindon TE. Association of periodontal disease and tooth loss with rheumatoid arthritis in the US population. The Journal of Rheumatology 2008; 35 (1): 70-76.
38. Bartold PM, Lopez-Oliva I. Periodontitis and rheumatoid arthritis: an update 2012-2017. Periodontology 2000 2020; 83 (1): 189-212. doi: 10.1111/prd.12300
39. Sculley DV, Langley-Evans SC. Salivary antioxidants and periodontal disease status. Proceedings of the Nutrition Society 2002; 61 (1): 137-143. doi: 10.1079/pns2001141
40. Soory M. Redox status in periodontal and systemic inflammatory conditions including associated neoplasias: antioxidants as adjunctive therapy? Infectious Disorders-Drug Targets 2009; 9 (4): 415-427. doi: 10.2174/187152609788922582
41. Larheim TA, Smith HJ, Aspestrand F. Rheumatic disease of the temporomandibular joint: MR imaging and tomographic manifestations. Radiology 1990; 175 (2): 527-531. doi: 10.1148/ radiology.175.2.2326477
42. Plant MJ, Williams AL, O’Sullivan MM, Lewis PA, Coles EC et al. Relationship between time-integrated C-reactive protein levels and radiologic progression in patients with rheumatoid arthritis. Arthritis & Rheumatism: Official Journal of the American College of Rheumatology 2000; 43 (7): 1473-1477. doi: 10.1002/1529-0131(200007)43:7˂1473::AIDANR9˃3.0.CO;2-N
43. Warren MP, Fried JL. Temporomandibular disorders and hormones in women. Cells Tissues Organs 2001; 169 (3): 187- 192. doi: 10.1159/000047881