• Users Online: 92
  • Home
  • Print this page
  • Email this page
Home About us Editorial board Ahead of print Current issue Search Archives Submit article Instructions Subscribe Contacts Login 


 
 Table of Contents  
ORIGINAL ARTICLE
Year : 2016  |  Volume : 2  |  Issue : 2  |  Page : 108-116

Study of chronic periodontitis in rheumatoid arthritis patients and its relation to serum anticitrulinated peptide antibody levels


1 Rheumatology Unit, Department of Internal Medicine, Faculty of Dentistry, University of Alexandria, Alexandria, Egypt
2 Department of Clinical and Chemical Pathology, Faculty of Medicine, Faculty of Dentistry, University of Alexandria, Alexandria, Egypt
3 Department Oral Medicine and Periodontology, Faculty of Dentistry, University of Alexandria, Alexandria, Egypt

Date of Submission17-May-2016
Date of Acceptance25-May-2016
Date of Web Publication5-Jan-2017

Correspondence Address:
Mona M Ashraf
Rheumatology Unit, Department of Internal Medicine, Faculty of Medicine, Alexandria University, Alexandria, Egypt, Tel: 002 01225087100;
Egypt
Login to access the Email id

Source of Support: None, Conflict of Interest: None


DOI: 10.4103/2356-8062.197573

Rights and Permissions
  Abstract 

Background
Recently discovered evidence suggests that periodontitis might have a direct role in initiating and sustaining the immunoinflammatory responses in rheumatoid arthritis (RA), besides the risk factors that are common to both conditions.
Aim
The aim of this study was to determine the prevalence of chronic periodontitis in a cohort of Egyptian RA patients and their first-degree relatives and siblings compared with a control group and its relation to serum anticitrulinated peptide antibody (ACPA) levels.
Patients and methods
This study was carried out on three groups: group I included 100 patients with RA who fulfilled the 2010 ACR/EULAR classification criteria for RA and had less than 5 years’ disease duration. They were recruited from the Rheumatology Unit and Rheumatology Outpatient Clinic at Alexandria Main University Hospital. Group II included 50 first-degree relatives and siblings of RA patients who were free of clinical joint disease, and group III included 50 age-matched and sex-matched healthy subjects referred for general dental treatment at the Dental Clinic of Alexandria Main University Hospital. RA disease activity was assessed by applying Disease Activity Score 28, and the functional state of the patients was assessed by applying the Health Assessment Questionnaire. All subjects underwent a dental examination, including Probing Pocket Depth (PPD), Clinical Attachment Loss (CAL), Plaque Index (PI), and modified Gingival Index. The ACPA levels in serum were evaluated in group I, group II, and group III participants with periodontitis.
Results
Group I patients had significantly more periodontitis than group II (P<0.001) and group III (P<0.001). There was a statistically significant difference between group I and group II in PPD (P<0.001), CAL (P<0.001), and PI (P<0.001) and a statistically significant difference between group I and group III in PPD (P=0.001), CAL (P=0.006), and PI (P=0.002). In group I, 82 (82%) patients had positive serum ACPA (320 U/ml), compared with only four (8%) subjects in group II and none of the controls in group III. There was a statistically significant difference between group I and group II in serum ACPA level (P<0.001), as well as between group I and group III (P<0.001).
Conclusion
Our study shows an association between RA and chronic periodontitis. Individuals with RA are more likely to experience periodontitis.

Keywords: anticitrulinated peptides antibodies, periodontitis, rheumatoid arthritis


How to cite this article:
Mahmoud RA, Hassab AH, Abdel Magid MH, Soliman EA, Fahmy RA, Ashraf MM. Study of chronic periodontitis in rheumatoid arthritis patients and its relation to serum anticitrulinated peptide antibody levels. Egypt J Obes Diabetes Endocrinol 2016;2:108-16

How to cite this URL:
Mahmoud RA, Hassab AH, Abdel Magid MH, Soliman EA, Fahmy RA, Ashraf MM. Study of chronic periodontitis in rheumatoid arthritis patients and its relation to serum anticitrulinated peptide antibody levels. Egypt J Obes Diabetes Endocrinol [serial online] 2016 [cited 2020 Jul 7];2:108-16. Available from: http://www.ejode.eg.net/text.asp?2016/2/2/108/197573


  Introduction Top


Rheumatoid arthritis (RA) is a chronic systemic autoimmune inflammatory disease that predominantly affects multiple peripheral joints. It is characterized by joint swelling and tenderness [1] resulting in progressive destruction of cartilage and bone in multiple joints [1].

Despite the recent advances in molecular pathogenesis its etiology is almost completely unknown. It is regarded as a complex multifactorial disease in which multiple genes and environmental factors act in concert to cause pathological events [2].

The potential impact of RA and many systemic disorders on the periodontium is well documented, and recent evidence suggests that periodontal infection may significantly enhance the risk for various systemic diseases including RA [3],[4].

Chronic periodontitis has been defined as ‘an infectious disease resulting in inflammation within the supporting tissues of the teeth, progressive attachment loss, and bone loss’ [5]. Periodontal pocket formation is usually a sequel of the disease process [6].

RA demonstrates remarkably similar patterns of soft-tissue and hard-tissue destruction as in chronic periodontitis. Chronic periodontitis shares a common immune inflammatory profile with RA [7],[8] and might have a direct causal role by initiating and sustaining the immune-mediated inflammatory response in RA, besides the genetic, environmental, and behavioral factors that are common to both conditions [9],[10],[11],[12],[13],[14].

Although the etiologies of these two chronic inflammatory diseases are separate, the underlying pathological processes are of sufficient similarity to warrant consideration of the hypothesis that individuals with RA are more likely to experience periodontitis and that the severity of periodontitis will be higher in RA patients [15].


  Patients and methods Top


This study was carried out on three groups: group I included 100 patients with RA fulfilling the 2010 ACR/EULAR [16] classification criteria for RA and of less than 5 years’ disease duration. They were recruited from those attending the Rheumatology Unit and Rheumatology Outpatient Clinic at the Alexandria Main University Hospital. Group II included 50 first-degree relatives and siblings of RA patients who were free of clinical joint disease, and group III included 50 age-matched and sex-matched healthy individuals who were referred for general dental treatment at the Dental Clinic of Alexandria Main University Hospital.

Informed consent from all patients was obtained as required by the Declaration of Helsinki before the commencement of the study. This study was approved by the Independent Ethics Committee.

Exclusion criteria included being a smoking, presence of diabetes mellitus, having undergone periodontal treatment (including prophylaxis) and/or antibiotic therapy over the past 3 months, having faulty prosthesis and fillings, and being pregnant or lactating.

RA disease activity was evaluated by applying the Disease Activity Score 28 (DAS 28), which involves four parameters [erythrocyte sedimentation rate (ESR) version] [17],[18],[19]. The functional state of the patients was assessed by applying the Health Assessment Questionnaire (HAQ) [20],[21].

All participants underwent a dental examination to detect and classify periodontal disease according to American Academy of Periodontology 1999 [22] on the basis of Probing Pocket Depth (PPD) [23], Clinical Attachment Loss (CAL) [23], Plaque Index (PI) [24], and modified Gingival Index (GI) [25].

Laboratory assessments included evaluation of acute-phase reactants, ESR, and C-reactive protein (CRP) levels.

Anticitrulinated peptide antibody (ACPA) levels in serum were evaluated for group I, group II, and group III with periodontitis by means of ELISA [26].

Statistical analysis

The data were analyzed statistically using the statistical package for the social sciences (SPSS software package, version 20.0; IBM; IBM Corp., Armonk, NY) and Microsoft excel (Microsoft; Microsoft Redmond campus, Redmond, Washington, United States). Qualitative data were described using number and percentage. Quantitative data were described using range (minimum and maximum), mean, SD, and median. The tests used were Spearman’s correlation coefficient, χ2-test, Mann–Whitney test, Kruskal–Wallis test, Fisher’s exact or Monte-Carlo test, and F-test (analysis of variance). P less than 0.05 was accepted as statistically significant.


  Results Top


Measures of disease activity and functional disability in rheumatoid arthritis patients

The disease activity state in RA patients was assessed by applying DAS 28 and every patient had a score that was a sum of different clinical and laboratory parameters. Two percent of patients were in remission, 2% had low disease activity, 34% had moderate disease activity, and 62% had high disease activity (mean DAS 28: 5.67±1.38) ([Table 1]).
Table 1: Measures of disease activity and functional disability in group I (rheumatoid arthritis patients) (n=100)

Click here to view


Functional disability was assessed using HAQ. Thirty-two percent of patients had no disability, 26% had mild disability, 8% had moderate disability, and 34% had severe disability (mean HAQ: 1.62±0.93).

Periodontal disease diagnosis and site-specific scores in periodontitis cases in a comparison between the studied groups

Group I patients had significantly more periodontitis than group II (P<0.001) and group III subjects (P<0.001); 66% of patients in group I had periodontitis compared with 22% of subjects in group II and 30% of subjects in group III. There was no statistically significant difference between group II and group III regarding affection with periodontitis (P=0.362) (Tables 2 and 3).
Table 3: Comparison between the studied groups according to site-specific scores in periodontitis cases

Click here to view


On comparing the studied groups regarding site-specific scores ([Table 3]), we found a statistically significant difference between group I and group II in PPD (P<0.001), CAL (P<0.001), and PI (P<0.001) and a statistically significant difference between group I and group III in PPD (P=0.001), CAL (P=0.006), and PI (P=0.002). No statistically significant difference between group II and group III in terms of PPD (P=0.938), CAL (P=0.135), or PI (P=0.504) was detected. No statistically significant difference was detected between the three studied groups with respect to GI (P=0.074).{Table 3}

In group I, the mean PPD was 4.88±1.43, mean CAL was 4.26±1.92, mean GI was 2.16±0.53, and mean PI was 2.17±0.62.

In group II, mean PPD was 2.76±0.78, mean CAL was 1.90±0.70, mean GI was 1.91±0.64, and mean PI was 1.50±0.45.

In group III, mean PPD was 3.10±1.05, mean CAL was 2.78±1.28, mean GI was 1.85±0.45, and mean PI was 1.65±0.31 ([Table 3]).

Measurement of serum anticitrulinated peptide antibody level and its comparison between periodontitis cases in the three studied groups

Serum ACPA levels were measured in all group I and group II subjects and in subjects with periodontitis in group III ([Table 4],[Table 5],[Table 6]).
Table 4: Comparison between the studied groups according to detection of serum anticitrulinated peptide antibody

Click here to view
Table 5: Comparison between the studied groups according to serum anticitrulinated peptide antibody level

Click here to view
Table 6: Positive serum anticitrulinated peptide antibody in periodontitis cases in the studied groups

Click here to view


In group I, 82 (82%) patients had positive serum ACPA (320 U/ml), compared with only four (8%) subjects in group II and none of the subjects in group III. There was a statistically significant difference between group I and group II (P<0.001) and between group I and group III (P<0.001). No statistically significant difference was detected between group II and group III (P=0.117) ([Table 4]).

The mean serum ACPA level in group I was 296.01±500.02 U/ml, that in group II was 7.42±9.35 U/ml, and that in group III was 9.04±5.72 U/ml. There was a statistically significant difference between group I and group II (P<0.001). A statistically significant difference was also detected between group I and group III (P<0.001). No statistically significant difference was detected between group II and group III (P=0.374) ([Table 5]).

Periodontitis was higher in ACPA-positive RA subjects, as 54 (81.8%) periodontitis cases in group I had positive serum ACPA compared with only two (18.2%) periodontitis cases in group II and none in group III. A statistically significant difference was detected between group I and group II (P<0.001) and between group I and group III (P2<0.001). No statistically significant difference was detected between group II and group III (P=0.169) ([Table 6]).

Correlation between anticitrulinated peptide antibody level in serum and Disease Activity Score 28, Health Assessment Questionnaire, erythrocyte sedimentation rate, C-reactive protein, and site-specific scores in group I patients with periodontitis

Serum ACPA was negatively correlated with DAS 28 and HAQ and all site-specific scores (PPD, CAL, GI, and PI), and positively correlated with ESR and CRP, but none was statistically significant (Tables 7 and 8).
Table 8: Correlation between serum anticitrulinated peptide antibody and site-specific scores in periodontitis cases in the studied groups

Click here to view


Correlation between anticitrulinated peptide antibody level in serum and site-specific scores in group II and group III subjects with periodontitis (Table 8)

In group II, there was a negative correlation between serum ACPA and PPD, CAL, and PI with no statistical significance. In contrast, the correlation between serum ACPA and GI was positive, but there was no statistical significance.

In group III, there was a significant negative correlation between serum ACPA and CAL (P<0.001) and PI (P=0.044). There was a positive correlation with PPD and negative correlation with GI, but none was of statistical significance.

Correlation between site-specific Clinical Attachment Loss and erythrocyte sedimentation rate

There was a significant positive correlation between site-specific CAL and ESR ([Figure 1]).
Figure 1: Correlation between site-specific Clinical Attachment Loss and erythrocyte sedimentation rate in periodontitis cases in group I (rheumatoid arthritis patients).

Click here to view


Correlation between site-specific scores and Disease Activity Score 28 in group I patients with periodontitis

There was a correlation between RA disease activity and periodontal disease severity and activity as reflected by positive significant correlation between DAS 28 and CAL and GI ([Figure 2] and [Figure 3]).
Figure 2: Correlation between Disease Activity Score 28 and site-specific Clinical Attachment Loss in periodontitis cases in group I (rheumatoid arthritis patients).

Click here to view
Figure 3: Correlation between Disease Activity Score 28 and site-specific Gingival Index in periodontitis cases in group I (rheumatoid arthritis patients).

Click here to view



  Discussion Top


Diseases like RA result in the (patho)physiological citrullination of structure proteins and in an increased accumulation of citrullinated proteins [27]. The reduced immunotolerance of these patients to citrullinated proteins seems to be a key problem, and hence there is an increased development of autoantibodies [27].

Whereas citrullination is associated with inflammation in general, the development of antibodies against them (ACPA) is specific to RA. The high specificity of ACPA is therefore most likely the result of an abnormal humoral response to these proteins. ACPA is produced locally in the inflamed synovium [28], suggesting that the resulting immune complexes are directly involved in the disease pathogenesis of the chronic inflammation in the rheumatoid joint. Whether there is local ACPA production in the periodontium and in the bronchoalveolar compartment still not established, despite high ACPA reactivity in serum samples of aggressive periodontitis patients has been reported [29].

Prevalence of periodontal disease and site-specific scores in periodontitis cases in a comparison between the studied groups

In our study, RA patients had significantly more periodontitis than did controls, as 66% of RA patients had periodontitis compared with 22% of subjects in group II and 30% of subjects in group III.

Although periodontal destruction is frequently seen among family members, suggesting a genetic basis for the susceptibility to periodontal disease [6], this was not detected in our study as there was no statistically significant difference between the control groups (II and III) regarding the prevalence of periodontitis. This may be due to the young age of group II subjects in our study. Also the familial background of group III subjects was not known.

To date, a large number of clinical studies [30],[31],[32],[33],[34],[35],[36],[37] have indicated a potential positive association between the occurrence of periodontitis and RA.

De Pablo et al. [37] found that RA patients had about a two-fold increase in periodontitis. Also, Mercado et al. [32] indicated that the incidence of RA in patients suffering from periodontitis is 3.95% compared with 1% prevalence in the general population.

Only few authors observed no association between the occurrences of these diseases [38].

In patients with RA, disability in the upper extremities of the body and reduced manual dexterity might impair oral hygiene and thereby increase the risk for caries, periodontitis, and tooth loss [39]. However, impaired oral hygiene is unlikely to fully explain the positive association between RA and periodontitis [36].

In the present study, RA subjects had more PPD (P<0.001) and CAL (P<0.001) compared with non-RA subjects, and the difference was statistically significant. No statistically significant difference was detected between group II and group III.

Regarding PPD, our study was similar to that of Abdelsalam et al. [40], as a statistically significant difference in the mean pocket depth between their study group (RA patients) and control group (age-matched and sex-matched healthy volunteers) was detected: a mean pocket depth greater than 4 mm was observed in 10% of the study group versus 1.25% of the control group, which indicated the presence of deeper pocket depth in RA patients.

These results also agreed with those of Mercado et al. [33], Mikael and Sigvard [41], Pischon et al. [36], and Mayer et al. [1].

The increased occurrence and severity of periodontitis in RA subjects compared with controls may be due to the common features of an underlying dysregulation of the inflammatory mechanism that predisposes these individuals to advanced, aggressive, and severe forms of either disease [7].

Regarding CAL, a significant difference was observed between our RA subjects and controls. The results agreed with those of Ishi Ede et al. [42], Mikael and Sigvard [41], and De Pablo et al. [37].

Our RA subjects had more plaque deposits than control groups. This was in agreement with the findings of Ishi Ede et al. [42] and Bozkurt et al. [43], who demonstrated a high prevalence of sites with dental plaque in their studies. This may be attributed to the fact that those patients directed their attention mainly at their serious illness while neglecting their oral health.

On the other hand, Abdelsalam et al. [40] found no statistically significant difference in the PI between their RA patients and the control group, which is in agreement with Mercado et al. [33] and Mayer et al. [1].

No significant difference was found in GI between the three studied groups in our study. We did not exclude any medications in our study; thus, RA cases were taking NSAIDs, which in turn reduces gingival inflammation [34].

This is similar to the findings reported by Mercado et al. [33] and Ishi Ede et al. [42], but it disagrees with the findings by Mayer et al. [1], who found a higher prevalence of sites with gingival inflammation in RA patients compared with the control group. Also, Kässer et al. [31] found greater gingival bleeding in RA subjects than in controls.

Some studies have failed to demonstrate meaningful differences in clinical indices of oral hygiene between individuals with or without RA [31],[33]. They related this to the fact that a single assessment of oral hygiene at a study visit might not reflect the long-term oral hygiene status of an individual [43].

In our study, there was a positive correlation between RA disease activity and periodontal disease severity and activity as reflected by a positive significant correlation between DAS 28 and both CAL and GI.

A positive significant correlation between CAL and ESR was also found.

This was in agreement with the findings of Abou-Raya et al. [35] and Kobayashi et al. [44], who have reported that periodontal disease severity goes hand in hand with RA disease activity.

Measurement of serum anticitrulinated peptide antibody level

Citrullination of proteins occurs under inflammatory conditions and results in the production of anticitrullinated antibodies. ACPA can be used as a marker of RA and is rarely present in the absence of RA (0–2%) [45].

Two studies, Pischon et al. [36] and Dissick et al. [46], investigated the levels of anticyclic citrullinated protein (anti-CCP) antibodies in periodontal and RA patients. One study reported anti-CCP antibody levels as a percentage, and the other reported the levels as U/ml. None of the studies reported statistically significantly higher levels of anti-CCP antibodies in patients with periodontal disease and RA. The results of these studies do not provide good evidence for a correlation between increased levels of anti-CCP antibodies and the presence of periodontal disease and RA [47].

A study of patients with RA and chronic periodontitis found an association between seropositivity for anti-CCP antibodies and increased severity of periodontitis [46].

In a recent study, a small group of patients with chronic periodontitis was examined for the presence of anti-CCP antibodies in serum, and only one patient out of 20 was found to be seropositive [48].

In the present study, positive serum ACPA (320 U/ml) was detected in 82% of RA patients and in only 8% of group II subjects; ACPA was not detected in group III subjects.

Periodontitis was higher in ACPA-positive RA subjects, as 81.8% of periodontitis cases in group I had positive serum ACPA. Only 18.2% in group II and none among periodontitis cases in group III had positive serum ACPA.

Serum ACPA levels did not correlate with RA disease activity (assessed by DAS 28), functional disability (using HAQ), ESR and CRP levels in RA patients, or with periodontal disease scores in periodontitis cases in the three studied groups.

In the periodontitis cases in group III, ACPA was absent in the serum. A short duration of periodontitis may be a possible explanation. These subjects should be followed up for development of serum ACPA.

In group II, four relatives had ACPA in their serum; two of them had periodontitis.

The presence of serum ACPA in first-degree relatives and siblings may precede the occurrence of RA and these subjects are considered at high risk for RA.


  Conclusion Top


In conclusion, our study shows an association between RA and chronic periodontitis. Individuals with RA are more likely to experience periodontitis. The CAL is higher in subjects with RA and correlates with RA disease activity. This may be due to a common genetic predisposition as both RA and chronic periodontitis are associated with the same HLA gene complex that regulates monocytic cytokine response. Chronic periodontitis shares a common immune inflammatory profile with RA, and both result from a common underlying disregulation of the host immunoinflammatory response.

Periodontium is a possible site for protein citrullination and hence autoantibody formation. Thus, careful screening of periodontitis subjects with a history of arthritis or arthralgia would be promising for the early detection and treatment of this chronic debilitating disease.

Financial support and sponsorship

Nil.Conflicts of interest

There are no conflicts of interest.

 
  References Top

1.
Mayer Y, Balbir-Gurman A, Machtei EE. Anti-tumor necrosis factor-alpha therapy and periodontal parameters in patients with rheumatoid arthritis. J Periodontol 2009; 80:1414–1420.  Back to cited text no. 1
    
2.
Klareskog L, Catrina AI, Paget S. Rheumatoid arthritis. Lancet 2009; 373:659–672.  Back to cited text no. 2
    
3.
Berthelot JM, Le Goff B. Rheumatoid arthritis and periodontal disease. Joint Bone Spine 2010; 77:537–541  Back to cited text no. 3
    
4.
Nesse W, Dijkstra PU, Abbas F, Spijkervet FK, Stijger A, Tromp JA et al. Increased prevalence of cardiovascular and autoimmune diseases in periodontitis patients: a cross-sectional study. J Periodontol 2010; 81:1622–1628.  Back to cited text no. 4
    
5.
Flemmig TF. Periodontitis. Ann Periodontol 1999; 4:32–38.  Back to cited text no. 5
    
6.
Novak MJ, Novak KF. Chronic periodontitis [Chapter 16]. In: Fermin A. Carranza, Jane L. Forrest, E. Barrie Kenney, Perry R. Klokkevold, Michael G. Newman, M. John Novak, Philip Preshaw, Henry H. Takei, Nadeem Y. Karimbux, editor. Carranza’s clinical periodontology. 11th ed. St Louis, MO: Elsevier Saunders; 2012.  Back to cited text no. 6
    
7.
Bartold PM, Marshall RI, Haynes DR. Periodontitis and rheumatoid arthritis: a review. J Periodontol 2005; 76(Suppl):2066–2074.  Back to cited text no. 7
    
8.
Marotte H, Farge P, Gaudin P, Alexandre C, Mougin B, Miossec P. The association between periodontal disease and joint destruction in rheumatoid arthritis extends the link between the HLA-DR shared epitope and severity of bone destruction. Ann Rheum Dis 2006; 65:905–909.  Back to cited text no. 8
    
9.
De Pablo P, Chapple IL, Buckley CD, Dietrich T. Periodontitis in systemic rheumatic diseases. Nat Rev Rheumatol 2009; 5:218–224.  Back to cited text no. 9
    
10.
Pincus T. Patient questionnaires and formal education as more significant prognostic markers than radiographs or laboratory tests for rheumatoid arthritis mortality − limitations of a biomedical model to predict long-term outcomes. Bull NYU Hosp Jt Dis 2007; 65(Suppl 1):s29–s36.  Back to cited text no. 10
    
11.
Borrell LN, Crawford ND. Social disparities in periodontitis among United States adults 1999-2004. Community Dent Oral Epidemiol 2008; 36:383–391.  Back to cited text no. 11
    
12.
Klareskog L, Padyukov L, Alfredsson L. Smoking as a trigger for inflammatory rheumatic diseases. Curr Opin Rheumatol 2007; 19:49–54.  Back to cited text no. 12
    
13.
Bergström J. Periodontitis and smoking: an evidence-based appraisal. J Evid Based Dent Pract 2006; 6:33–41.  Back to cited text no. 13
    
14.
Dietrich T, Maserejian NN, Joshipura KJ, Krall EA, Garcia RI. Tobacco use and incidence of tooth loss among US male health professionals. J Dent Res 2007; 86:373–377.  Back to cited text no. 14
    
15.
Joseph R, Rajappan S, Nath SG, Paul BJ. Association between chronic periodontitis and rheumatoid arthritis: a hospital-based case-control study. Rheumatol Int 2013; 33:103–109.  Back to cited text no. 15
    
16.
Aletaha D, Neogi T, Silman AJ, Funovits J, Felson DT, Bingham CO III et al. 2010 rheumatoid arthritis classification criteria: an American College of Rheumatology/European League Against Rheumatism collaborative initiative. Ann Rheum Dis 2010; 69:1580–1588.  Back to cited text no. 16
    
17.
Prevoo ML, van’t Hof MA, Kuper HH, van Leeuwen MA, van de Putte LB, van Riel PL. Modified disease activity scores that include twenty-eight-joint counts. Development and validation in a prospective longitudinal study of patients with rheumatoid arthritis. Arthritis Rheum 1995; 38:44–48.  Back to cited text no. 17
    
18.
Aletaha D, Landewe R, Karonitsch T, Bathon J, Boers M, Bombardier C et al. Reporting disease activity in clinical trials of patients with rheumatoid arthritis: EULAR/ACR collaborative recommendations. Ann Rheum Dis 2008; 67:1360–1364.  Back to cited text no. 18
    
19.
Van der Heijde DM, van’t Hof MA, van Riel PL, Theunisse LA, Lubberts EW, van Leeuwen MA et al. Judging disease activity in clinical practice in rheumatoid arthritis: first step in the development of a disease activity store. Ann Rheum Dis 1990; 49:916–920.  Back to cited text no. 19
    
20.
Da Mota Falcão D, Ciconelli RM, Ferraz MB. Translation and cultural adaptation of quality of life questionnaires: an evaluation of methodology. J Rheumatol 2003; 30:379–385.  Back to cited text no. 20
    
21.
Ferraz MB, Oliveira LM, Araujo PM, Atra E, Tugwell P. Crosscultural reliability of the physical ability dimension of the health assessment questionnaire. J Rheumatol 1990; 17:813–817.  Back to cited text no. 21
    
22.
Armitage GC. Development of a classification system for periodontal diseases and conditions. Ann Periodontol 1999; 4:1–6.  Back to cited text no. 22
    
23.
Glavind L, Loe H. Error in the clinical assessment of periodontal destruction. J Periodont Res 1967; 2:180–184.  Back to cited text no. 23
    
24.
Silness J, Loe H. Periodontal disease in pregnancy. II. Correlation between oral hygiene and periodontal condition. Acta Odontol Scand 1964; 22:121–135.  Back to cited text no. 24
    
25.
Lobene RR, Weatherford T, Ross NM, Lamm RA, Menaker L. A modified gingival index for use in clinical trials. Clin Prev Dent 1986; 8:3–6.  Back to cited text no. 25
    
26.
Swart A, Burlingame RW, Gürtler I, Mahler M. Third generation anti-citrullinated peptide antibody assay is a sensitive marker in rheumatoid factor negative rheumatoid arthritis. Clin Chim Acta 2012; 414:266–272.  Back to cited text no. 26
    
27.
Van Venrooij WJ, Vossenaar ER, Zendman AJ. Anti-CCP antibodies: the new rheumatoid factor in the serology of rheumatoid arthritis. Autoimmun Rev 2004; 3(Suppl 1): S17–S19.  Back to cited text no. 27
    
28.
Kinloch A, Lundberg K, Wait R, Wegner N, Lim NH, Zendman AJ et al. Synovial fluid is a site of citrullination of autoantigens in inflammatory arthritis. Arthritis Rheum 2008; 58:2287–2295.  Back to cited text no. 28
    
29.
Hendler A, Mulli TK, Hughes FJ, Perrett D, Bombardieri M, Houri-Haddad Y et al. Involvement of autoimmunity in the pathogenesis of aggressive periodontitis. J Dent Res 2010; 89:1389–1394.  Back to cited text no. 29
    
30.
Albandar JM. Some predictors of radiographic alveolar bone height reduction over 6 years. J Periodontal Res 1990; 25:186–192.  Back to cited text no. 30
    
31.
Kässer UR, Gleissner C, Dehne F, Michel A, Willershausen-Zönnchen B, Bolten WW. Risk for periodontal disease in patients with longstanding rheumatoid arthritis. Arthritis Rheum 1997; 40:2248–2251.  Back to cited text no. 31
    
32.
Mercado F, Marshall RI, Klestov AC, Bartold PM. Is there a relationship between rheumatoid arthritis and periodontal disease? J Clin Periodontol 2000; 27:267–272.  Back to cited text no. 32
    
33.
Mercado FB, Marshall RI, Klestov AC, Bartold PM. Relationship between rheumatoid arthritis and periodontitis. J Periodontol 2001; 72:779–787.  Back to cited text no. 33
    
34.
Abou-Raya A, Abou-Raya S, Abu-Elkheir H. Periodontal disease and rheumatoid arthritis: is there a link? Scand J Rheumatol 2005; 34:408–410.  Back to cited text no. 34
    
35.
Abou-Raya S, Abou-Raya A, Naim A, Abuelkheir H. Rheumatoid arthritis, periodontal disease and coronary artery disease. Clin Rheumatol 2008; 27:421–427.  Back to cited text no. 35
    
36.
Pischon N, Pischon T, Kröger J, Gülmez E, Kleber BM, Bernimoulin JP et al. Association among rheumatoid arthritis, oral hygiene, and periodontitis. J Periodontol 2008; 79:979–986.  Back to cited text no. 36
    
37.
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.  Back to cited text no. 37
    
38.
Sjöström L, Laurell L, Hugoson A, Håkansson JP. Periodontal conditions in adults with rheumatoid arthritis. Community Dent Oral Epidemiol 1989; 17:234–236.  Back to cited text no. 38
    
39.
Arneberg P, Bjertness E, Storhaug K, Glennås A, Bjerkhoel F. Remaining teeth, oral dryness and dental health habits in middle-aged Norwegian rheumatoid arthritis patients. Community Dent Oral Epidemiol 1992; 20:292–296.  Back to cited text no. 39
    
40.
Abdelsalam SK, Hashim NT, Elsalamabi EM, Gismalla BG. Periodontal status of rheumatoid arthritis patients in khartoum state. BMC Res Notes 2011; 4:460.  Back to cited text no. 40
    
41.
Mikael N, Sigvard K. Gingivitis and periodontitis are related to repeated high levels of circulating TNF alpha in patients with RA. J Periodontol 2008; 79:1689–1696.  Back to cited text no. 41
    
42.
Ishi Ede P, Bertolo MB, Bossa C Jr, Kirkwood KL. Periodontal condition in patients with RA. Braz Oral Res 2008; 22:72–77.  Back to cited text no. 42
    
43.
Bozkurt FY, Berker E, Akkuş S, Bulut S. Relationship between interleukin-6 levels in gingival crevicular fluid and periodontal status in patients with rheumatoid arthritis and adult periodontitis. J Periodontol 2000; 71:1756–1760.  Back to cited text no. 43
    
44.
Kobayashi T, Murasawa A, Komatsu Y, Yokoyama T, Ishida K, Abe A et al. Serum cytokine and periodontal profiles in relation to disease activity of rheumatoid arthritis in Japanese adults. J Periodontol 2010; 81:650–657.  Back to cited text no. 44
    
45.
Nishimura K, Sugiyama D, Kogata Y, Tsuji G, Nakazawa T, Kawano S et al. Meta-analysis: diagnostic accuracy of anti-cyclic citrullinated peptide antibody and rheumatoid factor for rheumatoid arthritis. Ann Intern Med 2007; 146:797–808.  Back to cited text no. 45
    
46.
Dissick A, Redman RS, Jones M, Rangan BV, Reimold A, Griffiths GR et al. Association of periodontitis with rheumatoid arthritis: a pilot study. J Periodontol 2010; 81:223–230.  Back to cited text no. 46
    
47.
Kaur S, White S, Bartold PM. Periodontal disease and rheumatoid arthritis: a systematic review. J Dent Res 2013; 92:399–408.  Back to cited text no. 47
    
48.
Atzeni F, Sarzi-Puttini P, Lama N, Bonacci E, Bobbio-Pallavicini F, Montecucco C, Caporali R. Anti-cyclic citrullinated peptide antibodies in primary Sjögren syndrome may be associated with non-erosive synovitis. Arthritis Res Ther 2008; 10:R51.  Back to cited text no. 48
    


    Figures

  [Figure 1], [Figure 2], [Figure 3]
 
 
    Tables

  [Table 1], [Table 2], [Table 3], [Table 4], [Table 5], [Table 6], [Table 7], [Table 8]



 

Top
 
 
  Search
 
Similar in PUBMED
   Search Pubmed for
   Search in Google Scholar for
 Related articles
Access Statistics
Email Alert *
Add to My List *
* Registration required (free)

 
  In this article
Abstract
Introduction
Patients and methods
Results
Discussion
Conclusion
References
Article Figures
Article Tables

 Article Access Statistics
    Viewed1101    
    Printed61    
    Emailed0    
    PDF Downloaded28    
    Comments [Add]    

Recommend this journal


[TAG2]
[TAG3]
[TAG4]