We aimed to analyse parameters defining carious disease in patients with rheumatoid arthritis (RA) and to evaluate potential correlations with inflammatory systemic parameters related to RA. Materials and method. We performed a complex clinical oral exam (DMFT, PI, RFR, RFS, CT) and inflammatory tests (ESR, C-reactive protein) and ASLO in seven patients known with RA. The results were statistically analyzed by SPSS 16 programs and Spearman`s correlation. The results showed a positive correlation between ASLO and DMFT, PI, CT, ESR and DMFT, PI, CT, C-reactive protein and variable: CT, PI; negative correlations were reported between ASLO and RFR, RFS, while C-reactive protein also associated with DMFT, RFR, RFS. Conclusions RA can influence the patient's cariogenic risk

AIDA CORINA BADESCU

CODRINA ANCUTA

CRISTINA IORDACHE

CRISTINA-ANGELA GHIORGHE

RODICA CHIRIEAC

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Romanian Journal of Oral Rehabilitation Vol.10, No.3 , July – September 2018  69 CORRELATIONS BETWEEN CARIOUS DISEASE AND INFLAMMATORY SYNDROME IN RHEUMATOID ARTHRITIS   CRISTINA-ANGELA GHIORGHE1, CRISTINA IORDACHE 1*, RODICA CHIRIEAC 2, AIDA CORINA BADESCU 1, CODRINA ANCUTA 3  1 ―Grigore T.Popa‖ University of Medicine and Pharmacy Iasi, Romania, Faculty of Dental Medicine 2  SANOCARE Medical Center, 3A Ghica Voda Str., 700469, Iasi, Romania 3. ―Grigore T. Popa‖ University of Medicine and Pharmacy, Iași, Romania, Faculty of Medicine, Rheumatology Department *Corresponding authors: Cristina Iordache e-mail: ccmiiordache@yahoo.com  ABSTRACT  We aimed to analyse parameters defining carious disease in patients with rheumatoid arthritis (RA) and to evaluate potential correlations with inflammatory systemic parameters related to RA. Materials and method. We performed a complex clinical oral exam (DMFT, PI, RFR, RFS, CT) and inflammatory tests (ESR, C-reactive protein) and ASLO in seven patients known with RA. The results were statistically analyzed by SPSS 16 programs and Spearman`s correlation. The results showed a positive correlation between ASLO and DMFT, PI, CT, ESR and DMFT, PI, CT, C-reactive protein and variable: CT, PI; negative correlations were reported between ASLO and RFR, RFS, while C-reactive protein also associated with DMFT, RFR, RFS. Conclusions RA can influence the patient's cariogenic risk. Key words: carious indices, ASLO, VSH, C-reactive protein  INTRODUCTION Current epidemiological researches have reported certain correlations between chronic inflammatory rheumatic disorders such as rheumatoid arthritis (RA) and spondylarthritis and the presence of chronic infection (e.g. chronic periodontitis).  Rheumatoid arthritis is the most frequent inflammatory rheumatic disease predominantly affecting the small joint of the upper and lower limbs in bilateral and symmetric pattern, but may involve any joint [1]. It is a chronic inflammatory systemic autoimmune disease with an unknown aetiology, developing 2 to 3 times more common in women than in men.  Rheumatoid arthritis is widely characterized by chronic inflammation (both local-synovial and systemic) as well as specific articular damage resulting in significant burden – chronic pain, disability and, even, early mortality [2]. The course of RA may be also different according to the presence or absence of several variables including genetic background, disease activity, serum autoantibody profile, and, finally, the severity of inflammatory process [3,4].  The antigenic background for RA remains still debatable; indeed it was proposed that autoimmune reaction would be triggered by infections with Mycoplasma or certain viruses (EBV, CMV, or a retrovirus) which would have similar epitopes with auto-antigens (shared epitope).  Although RA remains an autoimmune disease, the hallmark of the disease is governed by a persistent, self-maintained severe and chronic inflammatory event, encouraged by certain (auto)antigens or Romanian Journal of Oral Rehabilitation Vol.10, No.3 , July – September 2018  70 infectious super-antigens. Etiological, it appears to be the result of a combination of factors that include genetic predisposition and antigenic stimulation, possibly as a result of infection with microorganisms [6]. Aberrant immunity has also a central role in the pathobiology of RA, proven by activation of T and B- cells, as well as macrophages with increased synthesis of proinflammatory cytokines (IL-6, TNFα, IL-1β) and antibodies (rheumatoid factor as well as anti-cyclic citrullinated peptide antibodies, considered as RA biomarkers); moreover, RA susceptibility is typically associated with specific expression of MHC class II alleles. The aim of our study was to analyse parameters defining carious disease in patients with RA and to evaluate potential correlations with inflammatory systemic parameters related to RA, recognising that chronic inflammatory rheumatic conditions may be a risk factor for disease carious.  MATERIAL AND METHODS Seven patients known with RA were enrolled in our study.  We performed standard assessments, including (i) complex clinical oral examination with evaluation of several variables such as DMFT indices, IP, RFR, RFS, CT (Saliva Test Check Buffer (GC), in accordance with the protocols; and (ii) RA-related parameters focusing on inflammatory blood tests reflecting systemic inflammation (ESR, fibrinogen, C-reactive protein, ASLO).  Statistical analysis was conducted in SPSS-16, p<0.05; correlations between variable were assessed by Spearman`s test. RESULTS AND DISCUSSIONS We reported a positive correlation between ASLO and DMFT, the values of DMFT increasing together with increasing ASLO level; however, the correlation has not reached statistical significance (p=0.156) (Table 1).  Comparable results were described for ASLO and PI (Table 2), meaning a positive correlation, with no statistical significance (p=0.065).  Furthermore, ASLO also correlated with another variable, RFR; we report a negative correlation between the two variables: RFR decrease with increasing ASLO, also statistically not-significant (p=0.14) (Table 3). We obtained a statistically significantly negative correlation between RFS and ASLO, RFS decreasing with increasing of (p=0.03). In table 5 it was the positive correlation, statistically significantly, between the ASLO and CT variables, while tables 6 and 7 show the positive correlation between VSH and DMFT, respectively PI variable. The results are insignificantly statistical (VSH/DMFT: p=0.658; VSH/PI: p=0.403) There is a negative correlation between VSH and RFR, respectively RFS variables, as seen in tables 8 and 9. The results are insignificantly statistical (VSH/RFR: p=0.054; VSH/RFS: p=0.057). Table 10 shows a positive correlation between VSH and CT variables, the results were no significantly statistically (p=0.092). Finally, tables 11, 12, and 14 show negative correlations between serum concentrations of C reactive protein and DMFT, PI, RFR, RFS variables. All the results were no significantly statistically (Protein C/DMFT: p=0.445; Protein C/PI: p=1.000; Protein C/RFR: p=0.091; Protein C/RFS: p=0.734). There is a positive correlation between the C reactive protein and CT, PI variables. The results was no significantly statistically (CRP/CT: p=0.739; CRP/PI: p=1.000) (table 14). Romanian Journal of Oral Rehabilitation Vol.10, No.3 , July – September 2018  71  Table 1. Spearman`s Correlation values for ASLO and DMFT indices   Table 2. Spearman`s Correlation values for ASLO and PI indices  Table 3. Spearman`s Correlation values for ASLO and RFR indices   Table 4. Spearman`s Correlation values for ASLO and RFS indices  Table 5. Spearman`s Correlation values for ASLO and CT indices   Table 6. Spearman`s Correlation values for VSH and DMFT indices  Table 7. Spearman`s Correlation values for VSH and PI indices   Table 8. Spearman`s Correlation values for VSH and RFR indices  Table 9. Spearman`s Correlation values for VSH and RFS indices   Table 10. Spearman`s Correlation values for VSH and CT indices Correlations1.000 .598. .1567 7.598 1.000.156 .7 7Correlation CoefficientSig. (2-tailed)NCorrelation CoefficientSig. (2-tailed)NASLODMFTSpearman's rhoASLO DMFTCorrelations1.000 .725. .0657 7.725 1.000.065 .7 7Correlation CoefficientSig. (2-tailed)NCorrelation CoefficientSig. (2-tailed)NASLOPISpearman's rhoASLO PICorrelations1.000 -.617. .1407 7-.617 1.000.140 .7 7Correlation CoefficientSig. (2-tailed)NCorrelation CoefficientSig. (2-tailed)NASLORFRSpearman's rhoASLO RFRCorrelations1.000 -.921**. .0037 7-.921** 1.000.003 .7 7Correlation CoefficientSig. (2-tailed)NCorrelation CoefficientSig. (2-tailed)NASLORFSSpearman's rhoASLO RFSCorrelation is significant at the 0.01 level (2-tai led).**. Correlations1.000 .966**. .0007 7.966** 1.000.000 .7 7Correlation CoefficientSig. (2-tailed)NCorrelation CoefficientSig. (2-tailed)NASLOCTSpearman's rhoASLO CTCorrelation is significant at the 0.01 level (2-tai led).**. Correlations1.000 .206. .6587 7.206 1.000.658 .7 7Correlation CoefficientSig. (2-tailed)NCorrelation CoefficientSig. (2-tailed)NVSHDMFTSpearman's rhoVSH DMFTCorrelations1.000 .378. .4037 7.378 1.000.403 .7 7Correlation CoefficientSig. (2-tailed)NCorrelation CoefficientSig. (2-tailed)NVSHPISpearman's rhoVSH PICorrelations1.000 -.746. .0547 7-.746 1.000.054 .7 7Correlation CoefficientSig. (2-tailed)NCorrelation CoefficientSig. (2-tailed)NVSHRFRSpearman's rhoVSH RFRCorrelations1.000 -.741. .0577 7-.741 1.000.057 .7 7Correlation CoefficientSig. (2-tailed)NCorrelation CoefficientSig. (2-tailed)NVSHRFSSpearman's rhoVSH RFSCorrelations1.000 .681. .0927 7.681 1.000.092 .7 7Correlation CoefficientSig. (2-tailed)NCorrelation CoefficientSig. (2-tailed)NVSHCTSpearman's rhoVSH CTRomanian Journal of Oral Rehabilitation Vol.10, No.3 , July – September 2018  72  Table 11. Spearman`s Correlation values for Protein C and DMFT indices   Table 12. Spearman`s Correlation values for Protein C and PI indices  Table 13. Spearman`s Correlation values for Protein C and RFR indices   Table 14. Spearman`s Correlation values for Protein C and RFS indices   Table 15. Spearman`s Correlation values for Protein C and CT indices    We analysed serum inflammatory variables as well as cariogenic parameters in patients suffering from RA.  It is widely recognized that patients with chronic inflammatory immune rheumatic disorders, mainly RA but also ankylosing spondylitis, lupus, scleroderma, may develop oral disease such as periodontitis, mucosal lesions and dental caries. Thus, Ellis et al showed that marginal periodontitis may be associated with high levels of systemic inflammation – increased C-reactive protein, hyperfibrinogenemia, even moderate leucocytosis; surprisingly, after specific periodontal therapy, CRP serum concentration decreased significantly. To mention, serum concentration of this protein may be a marker of acute and/or inflammatory infectious reactions [7]. Another study published by Noack et al. presented that increased levels of CRP in patients with periodontal margins depend on the severity of the disease, even after taking into account potential confounders such as age, smoking, body mass index, triglycerides and cholesterol [8]. On the other hand, D'Aiuto et al. have confirmed that increased serum C-reactive protein levels in patients with marginal periodontitis can cause a higher level of cariogenic risk [9]. Also, D'Aiuto et al., in another study, showed that severe periodontitis may be associated with increased systemic inflammation. They evaluated the levels of reactive C protein, interleukin-6, total cholesterol and LDL-cholesterol in clinically healthy patients with periodontal disease, and observed that after two months of treatment, levels were significantly reduced [10]. Durak D. et al showed that immune Correlations1.000 -.347. .4457 7-.347 1.000.445 .7 7Correlation CoefficientSig. (2-tailed)NCorrelation CoefficientSig. (2-tailed)NPROTEINA_CDMFTSpearman's rhoPROTEINA_C DMFTCorrelations1.000 .000. 1.0007 7.000 1.0001.000 .7 7Correlation CoefficientSig. (2-tailed)NCorrelation CoefficientSig. (2-tailed)NPROTEINA_CPISpearman's rhoPROTEINA_C PICorrelations1.000 -.683. .0917 7-.683 1.000.091 .7 7Correlation CoefficientSig. (2-tailed)NCorrelation CoefficientSig. (2-tailed)NPROTEINA_CRFRSpearman's rhoPROTEINA_C RFRCorrelations1.000 -.159. .7347 7-.159 1.000.734 .7 7Correlation CoefficientSig. (2-tailed)NCorrelation CoefficientSig. (2-tailed)NPROTEINA_CRFSSpearman's rhoPROTEINA_C RFSCorrelations1.000 .156. .7397 7.156 1.000.739 .7 7Correlation CoefficientSig. (2-tailed)NCorrelation CoefficientSig. (2-tailed)NPROTEINA_CCTSpearman's rhoPROTEINA_C CTRomanian Journal of Oral Rehabilitation Vol.10, No.3 , July – September 2018  73 diseases, including RA, can cause important changes in the salivary glands, with repercussions on oral health [11]. Moreover, Dumitrescu. et al., in a 2006 study in a group of hospitalized, elderly patients, found that elevated salivary albumin was in direct correlation with creatine with increased C-reactive protein values and the risk of caryotic disease and periodontal, respectively [12]. Common oral manifestations in rheumatoid arthritis include Sjogren‘s syndrome and temporomandibular joint disease (TMD), and studies have suggested associations with periodontal disease in patients with rheumatoid arthritis [13]. In their study, Meheriar Chopra et al [14] observed that dental hygiene, indices value of RFS, DMFT and sIgA were modified at patients with RA. As already mentioned, a number of oral manifestations have been described in RA patients. These include the well-recognized association with Sjogren‘s and xerostomia, TMD, methotrexate-induced ulcers, and an increasing emphasis on periodontal disease [15]. Additionally, secondary Sjogren‘s in RA is associated with an increased caries risk [16,17].  On the other hand, the symptomatic treatment of the majority of chronic inflammatory rheumatic conditions require a nonsteroidal anti-inflammatory drug which can cause gingivitis or dental erosions (salicylates) or, if they also contain sugar, may increase the risk of caries. Moreover, several synthetic disease modifying anti-rheumatic, drugs such as methotrexate and sulphasalazine, can also lead to gingival bleeding, oral ulceration and salivary changes [18]. In our study we described correlations between the ASLO, VSH and CRP values, respectively, DMFS caries index values, RFR, RFS, CT and PI indices.  Positive correlations were recorded between the variables: CRP/CT, ESR/PI, ESR/CT, ESR/DMFT, ASLO/PI, ASLO/CT, ASLO/DMFT; the positive correlation between the ASLO variable and the CT variable was statistically significant p = 0.000. Negative correlations were recorded between CRP/RFS, CRP/RFR, CRP/DMFT, ESR/RFS, ESR/RFR, ASLO/RFS, ASLO/RFR; the negative correlation between the ASLO variable and the RFS variable was statistically significant p = 0.03. Further studies on larger cohort of RA patients but also on patients other chronic inflammatory rheumatic disorders should be performed in order to validate our findings.      CONCLUSIONS 1. We suggest that patients with RA and have high blood levels of inflammatory parameters, including ESR, C reactive protein and also ASLO may have an increased risk of carious disease.  2.Additionally, RA patients associate chronic periodontal inflammation, an abnormal oral hygiene due to significant hand disability and may develop frequently root caries.  REFERENCES 1. Matthias Schneider, Klaus Krüger, Rheumatoid Arthritis—Early Diagnosis and Disease Management, Dtsch Arztebl Int 2013: 110(27–28), 477−84. 2. Birch JT Jr, Bhattacharya S. Emerging trends in diagnosis and treatment of rheumatoid arthritis. Prim Care 2010: 37, 779-92. Romanian Journal of Oral Rehabilitation Vol. 10, No. 3, July- September 2018  74 3. Gossec L, Combescure C, Rincheval N, et al. Relative Clinical influence of Clinical, Laboratory, and Radiological Investigations in Early Arthritis on the Diagnosis of Rheumatoid Arthritis. Data from the French Early Arthritis Cohort ESPOIR. J Rheumatol 2010: 37, 2486-92. 4. Finckh A, Liang MH, van Herckenrode CM, de Pablo P. Long-term impact of early treatment on radiographic  progression in rheumatoid arthritis: A meta-analysis. Arthritis Rheum 2006: 55, 864-72. 5. Mercado F, Marshall RI, Klestov AC, Bartold PM. Is there a relationship between rheumatoid arthritis and periodontal disease? J.of Clin.Periodontol., 2000: 27, 267-272. 6. Behzad Heidari,  Rheumatoid Arthritis: Early diagnosis and treatment outcomes, Caspian J Intern Med 2011: 2(1), 161-170. 7. Ellis JS, Averley PA, Preshaw PM, Steele JG, Seymour RA, Thomason JM. Change in cardiovascular risk status after dental clearance. BMJ, 2007: May 12, 202(9), 543-4. 8. Noack B, Genco RJ, Trevisan M, Grossi S, Zambon JJ, De Nardin E. Periodontal infections contribute to elevated systemic C-reactive protein level. J. Periodontol., 2001: Sep, 72(9), 1221-7. 9. D'ajuto F, Ready D, Tonetti MS. Periodontal disease and c-reactive protein-associated cardiovascular risk. J.Periodontal res., 2004: Aug,39(4), 236-41. 10. D'ajuto F, Nibal IL, Parkar M, Suvan J, Tonetti MS. Short-term effects of intensive periodontal therapy  on serum inflammatory markers and cholesterol. J. Dent. Res., 2005: mar, 84(3), 269-73. 11. Durack D, Petersdorf R. Changes in the epidemiology of endocarditis. In Kaplan E., Tarranta A (eds): Infective Endocardititis-An American Heart Association Symposium. Dallas, American Heart Association,1977: 46. 12. Dumitrescu AL, Turea A, Gociu M, Galie L. Critical evaluation of the prevalence of rheumatoid arthritis and periodontal disease. Vol. Congres „Zilele facultăţii de Medicină dentară‖, ed. X-a, Iaşi, 2006: 142-144. 13. Clifton O. Bingham III, Malini Moni. Periodontal disease and rheumatoid arthritis: the evidence accumulates for complex pathobiologic interactions. Curr Opin Rheumatol. 2013: May 25(3), 345–353. 14. Meheriar Chopra, Sameer Jadhav, Anuradha Venugopalan, Vivek Hegde, Arvind Chopra. Salivary immunoglobulin A in rheumatoid arthritis (RA) with focus on dental caries: a cross-sectional study. Clinical Rheumatology, 2012: 31 (2), 247-250. 15. 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, 2971–2978. 16. 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, 70–76. 17. Ancuta C, Ghiorghe CA, Chirieac R, Ciocan Pendefunda AA, Iordache C. Specific Sialochemical and Sialometric Changes and Cariogenic Risk in Patients with Primary Sjogren's Syndrome.  Revista de Chimie 2017:  68 (9), 2135-2138.    18. Walton AG, Welbury RR, Thomason JM, Foster HE, Oral health and juvenile idiopathic arthritis: a review. Rheumatology 2000: 39, 550-555        

CORRELATIONS BETWEEN CARIOUS DISEASE AND INFLAMMATORY SYNDROME IN RHEUMATOID ARTHRITIS

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CORRELATIONS BETWEEN CARIOUS DISEASE AND INFLAMMATORY SYNDROME IN RHEUMATOID ARTHRITIS

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