Self-perceived oral health and periodontal parameters in chronic periodontitis patients with and without rheumatoid arthritis

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1 Journal of Investigative and Clinical Dentistry (2014), 5, 1 6 ORIGINAL ARTICLE Periodontics Self-perceived oral health and periodontal parameters in chronic periodontitis patients with and without rheumatoid arthritis Fawad Javed 1, Hameeda Bashir Ahmed 2, Abid Mehmood 3, Toshinari Mikami 4, Hans Malmstrom 5 & Georgios E. Romanos 6 1 Engineer Abdullah Bugshan Research Chair for Growth Factors and Bone Regeneration, 3D Imaging and Biomechanical Laboratory, College of Applied Medical Sciences, King Saud University, Riyadh, Saudi Arabia 2 Department of Dentistry, Al-Farabi Dental College, Riyadh, Saudi Arabia 3 Department of Dentistry, Jinnah Postgraduate Medical Centre, Karachi, Pakistan 4 Department of Pathology, Iwate Medical University, Iwate, Japan 5 Division of General Dentistry, Eastman Institute for Oral Health, University of Rochester, Rochester, NY, USA 6 Department of Dental Medicine, School of Dental Medicine, Stony Brook University, New York, NY, USA Keywords bleeding on probing, chronic periodontitis, rheumatoid arthritis, self-perceived, socioeconomic status. Correspondence Dr Fawad Javed, Engineer Abdullah Bugshan Research Chair for growth Factors and Bone Regeneration, 3D Imaging and Biomechanical Laboratory, College of Applied Medical Sciences, King Saud University, P.O. Box 60169, Riyadh 11545, Saudi Arabia. Tel: fawjav@gmail.com Received 18 February 2014; accepted 7 April doi: /jicd Abstract Aim: It is hypothesized that self-perceived oral health and periodontal status are worse in chronic periodontitis (CP) patients with rheumatoid arthritis (RA) compared to CP patients without RA. The aim of the present study was to assess self-perceived oral health and periodontal parameters in CP patients with and without RA. Methods: Fifty CP patients with RA and 50 CP patients without RA were included. Information regarding sociodemographic characteristics and selfperceived oral symptoms were collected using a questionnaire. Periodontal parameters (plaque index, bleeding on probing, probing depth, clinical attachment loss, number of missing teeth, and marginal bone loss) were recorded. Results: There was no significant difference in socioeconomic status, education status, self-perceived oral symptoms, and periodontal parameters among CP patients with and without RA. Conclusions: Self-perceived oral health and periodontal parameters are mainly governed by the intensity of CP, and the role of RA in this context seems to be rather secondary. Introduction Chronic periodontitis (CP) is characterized by an inflammatory process that jeopardizes the supporting structures of teeth. In general, the destruction of periodontal tissues is associated with an imbalance between the host response and pathogenic microorganisms and their products. However, more precisely, a homeostatic imbalance among proteolytic enzymes (e.g. neutrophils elastase) and their inhibitors (e.g. a-1antitrypsin) and reactive oxygen species and the antioxidant defense systems is believed to play an essential role in the pathogenesis of CP. 1 In addition, the increased production and accumulation of advanced glycation end-products (AGE) in the periodontal tissues of patients with CP promotes periodontal inflammation and alveolar bone loss by impairing the chemotactic and phagocytic function of polymorphonuclear leukocytes and producing destructive inflammatory cytokines. 2 Studies have reported that self-perceived oral health and CP are worse in immunocompromised patients, as compared to systemically-healthy individuals (controls). 3 7 Rheumatoid arthritis (RA) is an autoimmune disease of the joints characterized by the loss of articular cartilage and bone. 8 Suspected factors associated with the ª 2014 Wiley Publishing Asia Pty Ltd 1

2 Chronic periodontitis and rheumatoid arthritis F. Javed et al. pathophysiology of RA include exogenous infectious agents, endogenous substances (e.g. connective tissue proteins), and altered immunoglobulins. 9 Raised levels of AGE have been found in the serum and synovial fluid of patients with RA. 10 Furthermore, oxidative stress in synovial tissue and synovial fluid in patients with RA have also been associated with increased disease activity, bone erosion, and tissue damage. 11 However, the precise etiology of RA remains unknown. The relationship between CP and RA has been well reported. 12,13 Clinical studies have shown that the prevalence of CP is significantly high in patients with RA compared to controls However, self-reported oral health in patients with RA remains poorly addressed. Because the immune system is compromised in patients with RA, we hypothesized that self-perceived oral health and periodontal status (clinical and radiographic) are worse in patients with RA compared to CP patients without RA. The aim of the present study was to assess the self-perceived oral health and periodontal parameters among CP patients with and without RA. Materials and methods Ethical approval The study protocol was reviewed and approved by the research ethics review committee of the Jinnah Postgraduate Medical Centre, Karachi, Pakistan. Written, informed consent was obtained from all participants before their inclusion in the present study. Exclusion criteria The exclusion criteria encompassed the following: (a) tobacco smoking and chewing; (b) alcohol consumption; (c) malocclusion (overlapping teeth); (d) edentulous individuals; (e) presence of other disorders, including acquired immune deficiency syndrome, diabetes mellitus, hepatitis B, hepatitis C, renal disorders, and cardiovascular disorders. Study participants In total, 100 individuals (50 patients with RA and CP and 50 self-reported systemically-healthy patients with CP alone) were included. Patients with RA were recruited from the outpatient department of a local health-care center in Karachi, Pakistan. All patients with RA had been prescribed non-steroidal anti-inflammatory drugs (NSA- IDs) and antibiotics by their physicians. Patients with CP were recruited from the Department of Dentistry, Jinnah Postgraduate Medical Centre, Karachi, Pakistan. Diagnosis of RA and CP The diagnosis of RA was based on the American Rheumatology Association 1987 revised criteria, which are as follows: (a) morning stiffness in and around joints lasting at least 1 h before maximal improvement; (b) soft tissue arthritis of at least three joint areas observed by a rheumatologist; (c) arthritis of the proximal interphalangeal, metacarpophalangeal, or wrist joints; (d) symmetric arthritis; (e) rheumatoid nodules; (f) presence of rheumatoid factor; and (g) radiographic erosions and/or periarticular osteopenia in wrist and/or hand joints. 17 The definition of RA was based on the following criteria: (a) presence of criteria a b for more than 6 weeks; and (b) the presence of more than four criteria. 17 Interview questionnaire Information regarding age, sex, socioeconomic status (SES), education status (graduate level education), duration of RA, daily oral hygiene maintenance regimes, and last visit to a dentist were collected by a trained interviewer (AM) via a questionnaire. Periodontal examination All periodontal examinations were performed by one examiner (AM). The overall kappa for the intra-examiner reliability was Full mouth plaque index (PI), bleeding on probing (BOP), probing depth (PD), and clinical attachment loss (CAL) were measured at six sites (mesiobuccal, midbuccal, distobuccal, distolingual/palatal, midlingual/palatal, and mesiolingual/palatal) per tooth on all maxillary and mandibular teeth (excluding third molars). 18 PI and BOP scores were expressed as the percentage of positive sites, PD was measured to the nearest millimeter using a graded probe (Goldman/Fox Williams probe; Hu-Friedy, Chicago, IL, USA), and CP was defined as CAL 3 mm, PD 5 mm, and marginal bone loss (MBL) 3 mm in more than 30% of the sites. 4,19 21 MBL Digital panoramic radiographs were taken using a panoramic tomography machine (Kodak 8000C System; Carestream Dental LLC, Atlanta, GA, USA). The radiographs were viewed on a calibrated computer screen (Samsung SyncMaster digital TV monitor; Samsung, Seoul, Korea) using a software program (Image Tool 3.0 Program; Department of Dental Diagnostic Science, University of Texas Health Science Center, San Antonio, TX, USA). MBL was considered as the vertical distance from 2 mm below the cementoenamel junction (CEJ) to the most 2 ª 2014 Wiley Publishing Asia Pty Ltd

3 F. Javed et al. Chronic periodontitis and rheumatoid arthritis apical part of marginal bone. 4 MBL was measured on bilateral maxillary and mandibular premolars and molars by one investigator (AM). Bilateral maxillary and mandibular third molars and teeth surfaces where the CEJ and/or the bone crest were not clearly visible due to technical reasons (e.g. dental restorations, interproximal caries, overlapping of teeth, and/or poor radiographic quality) were excluded. Statistical analysis Statistical analysis was performed using SPSS (SPSS Statsoft version 18; SPSS, Tulsa, OK, USA). One-way ANOVA test was performed to determine whether or not the dependent variables (PI, BOP, CAL, PD, MBL, and number of missing teeth) were statistically-significantly correlated with the independent variables. For multiple comparisons, the Bonferroni post-hoc test was performed. Odds ratios (OR) with 95% confidence intervals were also calculated for self-perceived oral health and periodontal parameters among the groups. Multiple logistic regression analysis was performed to calculate the OR for periodontal parameters, while controlling for age and CP 9 RA interactions simultaneously. P-values less than 0.05 were considered statistically significant. Results Characteristics of the study population There was no significant difference in mean age, sex, SES, and education status among CP patients with and without RA. Among the patients with RA, the mean duration of RA was years. Ninety-four percent of patients with RA and 90% of patients with CP reported that they brushed their teeth once daily. Oral hygiene maintenance twice daily was reported by 6% of CP patients with RA and 10% of CP patients without RA (Table 1). Among the CP patients with RA, 20% reported to have visited a dentist within 1 year, whereas 80% reported to have visited a dentist more than 1 year ago. Twenty-four percent of CP patients without RA reported to have visited a dentist within 1 year, and 76% reported to have visited a dentist more than 1 year ago (Table 1). Periodontal parameters, number of missing teeth, and MBL There was no significant difference in PI, BOP, PD, CAL, number of missing teeth, and MBL among CP patients with and without RA (Table 2). Table 1. Sociodemographic characteristics of the study cohort CP patients with RA (n = 50) CP patients without RA (n = 50) Mean age (years) Sex (female) Duration of RA (years) Mean monthly income (US$) Education status: graduate level (% of individuals) Oral hygiene maintenance (% of individuals) Once daily Twice daily 6 10 Three times daily Last visit to a dentist (% of individuals) Within the past 1 month Within the past 3 months Within the past 6 months Within the past 12 months More than 12 months ago Group comparisons for self-perceived oral health among CP patients with and without RA The OR for self-perceived oral health among CP patients with and without RA are presented in Table 3. There was no significant difference in the self-perceived oral symptoms among CP patients with and without RA. Group comparisons for periodontal parameters among CP patients with and without RA There was no significant difference in periodontal parameters (PI, BOP, CAL, MBL, and PD) among CP patients with and without RA (Table 4). Table 2. Clinical periodontal parameters, number of missing teeth, and marginal bone loss in CP patients with and without RA CP Patients with RA (n = 50) CP Patients without RA (n = 50) Plaque index (%) Bleeding on probing (%) Probing depth (in mm) Clinical attachment loss (in mm) No. missing teeth Marginal bone loss (in mm) ª 2014 Wiley Publishing Asia Pty Ltd 3

4 Chronic periodontitis and rheumatoid arthritis F. Javed et al. Table 3. Comparison of self-perceived oral health among CP patients with and without RA, and healthy controls (n = 464) Self-perceived oral symptoms Study participants Yes No Odds ratios (95% confidence intervals) P-value Bleeding gums CP patients with RA ( ) 0.38 CP patients without RA Pain in teeth CP patients with RA ( ) 0.57 CP patients without RA Pain on chewing CP patients with RA ( ) 0.12 CP patients without RA Loose teeth CP patients with RA ( ) 0.58 CP patients without RA Bad breath CP patients with RA ( ) 0.55 CP patients without RA Table 4. Group comparisons for periodontal parameters among CP patients with and without RA Group comparisons for periodontal variables Group mean difference (%) 95% confidence intervals of mean group difference P-value Plaque index (percentage sites) CP patients with RA vs CP patients without RA = Bleeding on probing (percentage sites) CP patients with RA vs CP patients without RA = Probing depth (mm) CP patients with RA vs CP patients without RA = Clinical attachment loss (mm) CP patients with RA vs CP patients without RA = Marginal bone loss (mm) CP patients with RA vs CP patients without RA = Discussion The present results demonstrated no significant difference in self-perceived oral health and clinical periodontal parameters (PI, BOP, CAL, PD, MBL, and number of missing teeth) in CP patients with and without RA. These results could be explained by various pathophysiological mechanisms (e.g. increased production and accumulation of AGE in the periodontal tissues, imbalance in the gingival crevicular fluid [GCF] pro-inflammatory and anti-inflammatory cytokines, and oxidative stress in periodontal tissues) that might have been concurrently occurring in the periodontal tissues of CP patients with and without RA. 12,22,23 Our results are in accordance with those of previous studies. 12,24,25 With regard to RA, mechanisms similar to those associated with the pathophysiology of CP (e.g. increased production of AGE in synovial tissues, oxidative stress in the synovial tissues, and imbalance between pro-inflammatory and anti-inflammatory cytokines in the synovial fluid) have been proposed. 2,11,14,26,27 We therefore expected selfperceived oral health and periodontal parameters to be worse in CP patients with RA compared to CP patients without RA. However, the present results showed no significant difference in self-perceived oral health and periodontal parameters among CP patients with and without RA. These present clinical results are in accordance with the outcomes of previous immunological studies, where no significant difference was observed in the GCF interleukin (IL)-1b levels among CP patients with and without type 2 diabetes mellitus In the present study, most of the CP patients with and without RA reported to brush their teeth once daily and had visited an oral health-care center over 1 year ago. However, upon periodontal examination, CP patients (with and without RA) had comparable clinical and radiographic periodontal parameters. Moreover, the SES and education status of CP patients with and without RA were comparable. It is therefore questionable whether or not these patients were persistently following their daily oral hygiene maintenance regimes. Raised clinical periodontal inflammatory parameters (BOP and CAL) in CP patients (with and without RA) might increase the levels of pro-inflammatory cytokines (e.g. IL-1b, IL-6, IL-17 and tumor necrosis factor-a [TNF-a]) in the GCF, thereby worsening the periodontal inflammatory conditions and ultimately causing MBL (if 4 ª 2014 Wiley Publishing Asia Pty Ltd

5 F. Javed et al. Chronic periodontitis and rheumatoid arthritis left uncontrolled). 28,31,32 The present study supports the results of a recent study, 22 which reported no significant differences in the GCF levels of IL-1b, IL-4, IL-10, and TNF-a among CP patients with and without RA. This suggests that the quality of self-rated oral health and the severity of periodontal parameters is chiefly governed by the severity of CP in patients with and without RA. It has been reported that NSAIDs act as inhibitors of the inflammatory destruction in periodontal disease. 33 An interesting finding in the present study was that, although antibiotics and NSAIDs have been prescribed to RA patients by their health-care providers, periodontal parameters (e.g. PD and gingival bleeding) remained comparable between CP patients with and without RA. It has been reported that an underprivileged SES and poor education status might compel patients to neglect their oral and systemic health and primarily focus on attaining basic standards of living. 4 Furthermore, underprivileged SES and poor education status might also convince patients to seek non-conventional therapies (including homeopathic, herbal, and/or spiritual therapies) than medically-approved allopathic therapeutic regimes for the treatment of systemic disorders. 4 We postulate that the patients in our study cohort were either unable to abide by the medication protocol/s recommended by their physicians for the treatment of RA or adopted non-conventional therapeutic regimes due to deprived living conditions or poor education status, or a combination of both. Within the limits of the present investigation, we conclude that the self-perceived oral health and periodontal parameters seem to be mainly governed by the intensity of CP, and the role of RA in this context is rather secondary. Acknowledgment The authors thank Professor David W. Paquette, Associate Dean of Education, School of Dental Medicine, Stony Brook University, New York, USA, for his guidance in developing the present manuscript. References 1 Bauer V, Bauer F. Reactive oxygen species as mediators of tissue protection and injury. Gen Physiol Biophys 1999; 18Spec No: Zizzi A, Tirabassi G, Aspriello SD, Piemontese M, Rubini C, Lucarini G. Gingival advanced glycation end-products in diabetes mellitus-associated chronic periodontitis: an immunohistochemical study. J Periodontal Res 2013; 48: Javed F, Tenenbaum HC, Nogueira- Filho G et al. Periodontal inflammatory conditions among gutka-chewers and non-chewers with and without prediabetes. J Periodontol 2013; 84: Javed F, Nasstrom K, Benchimol D, Altamash M, Klinge B, Engstrom PE. Comparison of periodontal and socioeconomic status between subjects with type 2 diabetes mellitus and nondiabetic controls. J Periodontol 2007; 78: Javed F, Al-Askar M, Samaranayake LP, Al-Hezaimi K. Periodontal disease in habitual cigarette smokers and nonsmokers with and without prediabetes. Am J Med Sci 2013; 345: Javed F, Al-Askar M, Al-Rasheed A, Babay N, Galindo-Moreno P, Al-Hezaimi K. Comparison of selfperceived oral health, periodontal inflammatory conditions and socioeconomic status in individuals with and without prediabetes. Am J Med Sci 2012; 344: Javed F, Sundin U, Altamash M, Klinge B, Engstrom PE. Self-perceived oral health and salivary proteins in children with type 1 diabetes. J Oral Rehabil 2009; 36: Lee DM, Weinblatt ME. Rheumatoid arthritis. Lancet 2001; 358: Mercado FB, Marshall RI, Bartold PM. Inter-relationships between rheumatoid arthritis and periodontal disease. A review. J Clin Periodontol 2003; 30: Tam LS, Shang Q, Li EK et al. Serum soluble receptor for advanced glycation end products levels and aortic augmentation index in early rheumatoid arthritis a prospective study. Semin Arthritis Rheum 2013; 42: Kundu S, Ghosh P, Datta S, Ghosh A, Chattopadhyay S, Chatterjee M. Oxidative stress as a potential biomarker for determining disease activity in patients with rheumatoid arthritis. Free Radic Res 2012; 46: Sezer U, Erciyas K, Ustun K et al. Effect of chronic periodontitis on oxidative status in patients with rheumatoid arthritis. J Periodontol 2013; 84: 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: Esen C, Alkan BA, Kirnap M, Akgul O, Isikoglu S, Erel O. The effects of chronic periodontitis and rheumatoid arthritis on serum and gingival crevicular fluid total antioxidant/oxidant status and oxidative stress index. J Periodontol 2012; 83: Pischon N, Pischon T, Kroger J et al. Association among rheumatoid arthritis, oral hygiene, and periodontitis. J Periodontol 2008; 79: Havemose-Poulsen A, Westergaard J, Stoltze K et al. Periodontal and hematological characteristics associated with aggressive periodontitis, juvenile idiopathic arthritis, and rheu- ª 2014 Wiley Publishing Asia Pty Ltd 5

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