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 Table of Contents  
ORIGINAL ARTICLE
Year : 2017  |  Volume : 15  |  Issue : 4  |  Page : 312-318

Association between periodontal disease temporomandibular disorders and rheumatoid arthritis among patients visiting rheumatology centers in Bengaluru City: A cross-sectional study


Department of Public Health Dentistry, Government Dental College and Research Institute, Bengaluru, Karnataka, India

Date of Web Publication13-Dec-2017

Correspondence Address:
Dr. Vijay Kumar
Room No. 9, Department of Public Health Dentistry, Government Dental College and Research Institute, Bengaluru - 560 002, Karnataka
India
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/jiaphd.jiaphd_125_17

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  Abstract 

Introduction: Association between rheumatoid arthritis (RA), periodontitis and temporomandibular disorder (TMD) can be an outcome of the existing inflammatory conditions or involvement of joints at a different level of severity. Aim: This study aims to find an association between periodontal disease and TMDs and RA among patients visiting various Rheumatology centers in Bengaluru city. Materials and Methods: A total of 100 RA patients and age- and gender-matched comparison group were recruited from various Rheumatology centers in Bengaluru city. Periodontal status and loss of attachment (LOA) were measured from the World Health Organization (2013) criteria and TMDs and severity were assessed using Helkimo index (1987). Data were analyzed and comparisons were done using Chi-square test and independent t-test (P < 0.05). Correlation and association are measured through spearman's correlation and logistic regression analysis. Results: There was a significant difference regarding shallow and deep periodontal pocket depth among RA (4.62 ± 2.33, 1.48 ± 1.7) and comparison (3.48 ± 2.53, 0.83 ± 1.05) groups (P = 0.01). Impaired mobility (P = 0.012), altered function (P = 0.032), painful function (P = 0.023), muscle pain (P = 0.028), and temporomandibular joint pain (P = 0.048) differed significantly between RA group and comparison group. RA patients were more likely to suffer from TMD (OR = 4.88) and LOA (OR = 2.16) than the comparison group. Conclusion: Periodontitis and TMD are found to be associated with RA. A dental check-up for patients suffering from RA should be part of the routine RA assessment.

Keywords: Arthritis, Helkimo index, periodontal attachment loss, periodontal pocket, rheumatoid, temporomandibular joint disorders


How to cite this article:
Kumar V, Yashoda R, Puranik MP. Association between periodontal disease temporomandibular disorders and rheumatoid arthritis among patients visiting rheumatology centers in Bengaluru City: A cross-sectional study. J Indian Assoc Public Health Dent 2017;15:312-8

How to cite this URL:
Kumar V, Yashoda R, Puranik MP. Association between periodontal disease temporomandibular disorders and rheumatoid arthritis among patients visiting rheumatology centers in Bengaluru City: A cross-sectional study. J Indian Assoc Public Health Dent [serial online] 2017 [cited 2020 Dec 5];15:312-8. Available from: https://www.jiaphd.org/text.asp?2017/15/4/312/220706

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  Introduction Top


The growth of scientific evidence suggests an exquisite association between oral infection and systemic diseases. A number of chronic conditions of altered connective tissue metabolism, hormone imbalance, and altered immune function have likewise been associated with increased risk of oral diseases.[1] Rheumatoid arthritis (RA) is one of the kind of inflammatory arthritis which has distinct effects on oral health.[2]

RA is a systemic, inflammatory autoimmune disorder in which multiple genes and environmental factors act in concert to cause pathologic events. Genetic effects appear to be augmented by exposure to environmental factors (i.e., smoking and infection), which might explain the occurrence of the disease.[3] Meta-estimates of regional RA prevalence rates for countries of low- or middle-income were 0.40% for Southeast Asian, 0.37% for Eastern Mediterranean, 0.62% for European, 1.25% for American, and 0.42% for Western Pacific regions. Indian Council of Medical Research 2012 survey reported a prevalence of RA 0.7% in India.[4],[5],[6]

RA is characterized by the accumulation and persistence of inflammatory infiltrates in the synovial membrane, joints, tendons, and periarticular structures.[7] The frequency of the temporomandibular disorders (TMD) in RA varies from 4.7% to 85%. A wide variation might be due to the diverse selection criteria and differences in the utilized evaluation methods. Besides pain and limitations of jaw function due to the limitation of condylar movement, an anterior opening of the bite due to articular cartilage and bone tissue destruction may develop among RA patients. However, the interaction between the systemic inflammatory activity and TMD is not yet clearly understood.[8]

The involvement of bone and connective tissue, host's immune system and function of neutrophils play a significant role in RA as well as in periodontitis. Polymorphism of interleukin (IL) 1α, IL1 β, and IL4 genes has been observed in both RA and periodontitis.[9] Association of HLA-DR4 alleles in genetic structure of RA and aggressive periodontitis patients are among other similarities of these conditions.[10] The use of nonsteroidal anti-inflammatory drugs for the treatment of RA decreases the progression of periodontal disease (PD) and associated bone loss in patients suffering from arthritis. Although the etiologies of these diseases are distinctly separate, the underlying pathological processes are of sufficient similarity to warrant consideration of the hypothesis that individuals at risk of developing RA may also be at risk of developing periodontitis, or vice versa.[11]

There seems to be an association among all three diseases, and they have strong similarities in the underlying pathologic processes and analogs mechanisms of tissues destruction. In previous studies, RA was found to be associated with periodontitis and TMD.[12],[13] This can be an outcome of the existing inflammatory conditions or involvement of joints at different level of severity or may be the upper limb movement limitations that result in patients' decreased ability to maintain their oral and dental hygiene and development of disease. However, the existence of these conditions concomitantly on epidemiological basis is not clear. Therefore, the aim of this study was to determine an association between PD and TMDs and RA among subjects visiting Rheumatology centers in Bengaluru city. It was hypothesized that there was no association between PD, TMDs, and RA.


  Materials and Methods Top


A cross-sectional comparative study was conducted among patients visiting Rheumatology centers from April to October 2016, in Bengaluru city. Ethical approval for the study was obtained from the Institutional Ethics committee, (Ethical approval No. GDCRI/ACM (2)/PG/PHD/S/2016-17) and informed consent was obtained from the participants.

The consistency of diagnostic criteria and intraexaminer variability were checked by re-examining subjects on different days. The Kappa coefficient value (κ) for intraexaminer reliability for the investigator was 0.86–0.90. The overall intraexaminer reliability was good and these values reflected high degree of conformity in observation

The sample size calculation was performed based on the prevalence of periodontitis in patients in the pilot study (80%) (α = 0.05, β = 0.20). Hence, a sample size of 100 in each RA and 100 age- and gender-matched comparison group was achieved by including participants visiting Rheumatology centers. Participants aged 18 years and above diagnosed with RA were included. Participants with cognitive impairment, systemic diseases/conditions which affect periodontal health and temporomandibular joint (TMJ), had undergone periodontal treatment (including prophylaxis), TMJ therapy and antibiotic therapy over the past 3 months were excluded from the study.

Demographic profile, medical history, dental history, oral hygiene practices, and diet history of study participants were recorded. Assessment of PD was done using Community Periodontal Index (CPI) and loss of attachment (LOA) by the World Health Organization (WHO) Oral Health Assessment Form for Adults, 2013.[14]

TMDs were evaluated using Helkimo index (1987)[15] which is a clinical dysfunction index that considers a functional evaluation of the masticatory system. In accordance with the presence and/or severity of these clinical symptoms, individuals are assigned a score of 0, 1, or 5.

The following items were recorded: 1-range of mandibular motion or impaired mobility; 2-TMJ function impairment or altered function; 3-painful function during different type of mandibular movement; 4-muscle pain during palpation; and 5-TMJ pain during palpation. Clinical dysfunction of TMD as assessed by the total Helkimo index scores were categorized into groups.

Dysfunction group 0 included absence of clinical symptoms with total score 0; dysfunction group 1 included minor dysfunction with total score 1–4; dysfunction group 2 included moderate dysfunction with total score 5–9; dysfunction group 3 included severe dysfunction with total score 10–13; severe dysfunction with total score 15–17; dysfunction group 5 included severe dysfunction with total score 20–25.

The study participants were comfortably seated on a chair and examined by a single calibrated investigator under artificial light and recording was done by the trained personnel in the respective centers after the study pro forma being coded (RA present or absent) by other investigator.

The data collected were entered into Excel spreadsheet after decoding the study pro forma and were analyzed using the Statistical Package for Social Sciences (SPSS) version 22 (SPSS Inc., Chicago, IL, USA).

The descriptive and inferential analysis was done. Independent t-test was used to found out the difference in mean scores between clinical variables. Chi-Square Test was used to find out the difference between proportions. Spearman's correlation was done to determine correlation among PD, TMD, and duration of RA disease. Logistic regression was applied to check the relationship between PD and TMDs. For this, data were categorized into TMD absent (dysfunction group 0, 1) and TMD present (dysfunction group 2–5); periodontitis absent (Code 0) and periodontitis present (Code 1–4). Statistical significance was considered at P < 0.05 (confidence interval [CI] of 95%).


  Results Top


The age of the participants ranged from 45 to 75 years. Mean age among RA group was 45.94 ± 9.90 years and in control group was 46.45 ± 10.62 years. There was no significant difference in tobacco habits, past dental visits, and treatment taken for dental problems. Vegetarian diet was preferred by RA group participants compared to mixed diet among comparison group (P = 0.004). Duration of the disease was <7 years in two-third of the participants, among those 15% were males and 50% were females. About 58% participants among RA group, who had duration ≤6 months were under nonsteroidal anti-inflammatory drugs (NSAIDs) and >6 months were on immunosuppressant or combination of these medications. Participant's characteristics of the RA and comparison group are shown in [Table 1].
Table 1: Participants characteristics among study groups

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There was no significant difference regarding mean number teeth with gingival bleeding (P = 0.458) between RA and comparison group. Mean number of teeth with shallow pockets (4–5 mm) were significantly higher among RA group (4.62 ± 2.33) than the comparison group (3.48 ± 2.53) (P = 0.001). Mean number of teeth with deep pocket (6 mm or more) were significantly higher among RA group (1.48 ± 1.7) than the comparison group (0.83 ± 1.05) (P = 0.002) [Table 2]. There was significant difference regarding the mean number of sextants with LOA affected per person with code 0 (P = 0.004), code 1 (P = 0.013), code 2 (P = 0.001), and code 3 (P = 0.003). However, no differences were found in code 4 and excluded sextant between RA and comparison group [Table 3].
Table 2: Mean number of teeth with periodontal disease indicators

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Table 3: Mean number of sextants with loss of attachment among study participants

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Clinical dysfunction of TMD as assessed by the Helkimo index. There was significant difference between RA and comparison group regarding impaired mobility (P = 0.012), altered function (P = 0.032), painful function (P = 0.023), muscle pain (P = 0.028), and TMJ pain (P = 0.048) [Table 4].
Table 4: Distribution of the study participants according to temporomandibular joint disorders

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Helkimo index scores were categorized into six dysfunction groups. There was significant difference between RA and comparison group regarding severity of TMJ disorders (P = 0.001). Prevalence with dysfunction group 0 and 1 disorders was less observed among RA than comparison group while dysfunction groups 2–4 were more observed among RA than comparison group. Dysfunction group 5 was seen in RA group only [Table 5].
Table 5: Distribution of the study participants according to severity of temporomandibular disorders

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There was significant moderate positive correlation between duration of disease and severity of TMD (r = 0.649) (P = 0.001). There was significant weak positive correlation between duration of disease and periodontitis (r = 0.308; P = 0.02), between severity of TMD and LOA among RA group (r = 0.22; P = 0.02). However, it was not significant among comparison group [Table 6].
Table 6: Correlation between loss of attachment and temporomandibular disorders among rheumatoid arthritis and comparison group

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Logistic regression analysis showed significant association present between RA disease, periodontitis, and TMD among study participants. RA group was twice more likely to have periodontitis than the comparison group (2.16 [95%, CI 1.18–3.65] P = 0.012). RA group was four time more likely to have TMD as than the comparison group (4.8 [95%, CI 2.60–8.59] P = 0.001) [Table 7].
Table 7: Logistic regression analysis of rheumatoid arthritis, periodontitis and temporomandibular disorders among study participants

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  Discussion Top


In the past decade, a growing body of evidence showed an association between RA and periodontitis. Although studies in RA patient show occurrence of TMD, the prevalence, extent, and severity of TMD related to RA is not clear on the epidemiological basis. There is a cross susceptibility between these diseases and remarkable similarities in the pathogenesis, inflammatory host response governed by immunogenic, thus providing useful insights into these diseases.[12],[13]

Cross-sectional studies,[2],[9],[11],[16],[17],[18],[19],[20],[21],[22],[23],[24] case–control studies,[25],[26] and systematic reviews and meta-analysis [12],[13] have investigated a possible association between RA and periodontitis, whereas a few studies have investigated the association between RA and TMDs.[27],[28],[29] Most of the previous studies have assessed either of the two variables in association with RA. However, one study described the prevalence and severity of TMDs and PD among patients with RA.[27] Hence, the association between these three variables needs to be explored.

In the majority of the previous studies, periodontitis was measured through objective measurement of clinical parameters such as probing depth.[9],[11],[16],[17],[18],[19],[26] clinical attachment level (CAL)[9],[11],[16],[17],[18],[19],[21],[22] and community periodontal index of treatment need.[18] In the current study, CPI with LOA, according to WHO (2013)[14] was used since the assessment of periodontitis is simple and as sensitive as clinical measurement and useful in epidemiological surveys. A standardized classification for TMJ disorder's signs and symptoms and the use of indices is an excellent means to allow disease severity to be individually classified to examine the prevalence of such problem in a specific population and measure the effectiveness of the therapies employed. Helkimo index [15] is used to measure the severity of TMJ disorders, as well as pain in this system.

RA has a peak incidence of onset in the fourth and fifth decades of life.[1],[5],[6] More than half of the participants (54%) were in 45–75 years of age group. The mean age of the RA group was 45.94 ± 09.90 years, which is in line with previous studies (42.7–62.5) years.[2],[7],[8],[9],[10],[11],[12],[13],[16],[17],[18],[19],[20],[21],[22],[23],[24],[25],[26],[27],[28],[29]

RA is three times more common in women than in men. This can be attributed to hormonal changes, fat distribution, and more fibrous joints among females. Steroid hormones are implicated to play an important role as modulation of autoimmune diseases such as RA. Estrogen and progesterone are joint protective hormones in females. Conditions such as postpartum and menopause, there is definite reduction in the concentration of these two hormones, which leads to middle-to-old aged women more susceptible to RA compare to men. Central adiposity among middle to old aged women have more weights on joints and leads to joint erosion and make it more susceptible to RA.[7],[14] In the present study, about 71% of the participants were females in RA group. The higher proportions of female patients in this study are in accordance with the natural history of the RA disease and also in line with the previous literatures (62%–100%).[2],[7],[8],[9],[10],[11],[12],[13],[16],[17],[18],[19],[20],[21],[22],[23],[24],[25],[26],[27],[28],[29]

Tobacco consumption is one of the main environmental influences for the development of RA among adults. As inflammatory conditions in the lungs of cigarette smokers were suggested to contribute to the breakdown of immune tolerance to citrullinated epitopes, chronic exposure to citrullinated proteins in patients with periodontitis may also predispose susceptible individuals to the development of autoantibodies and the initiation of RA. The risk of developing RA was approximately twice as high for smokers than for nonsmokers. For female smokers, the risk was approximately 1.3 times higher than for nonsmokers. Shin et al. suggested that smoking is indeed a risk factor for RA in RF-positive men and heavy smokers.[30] In the present study, there was no significant difference between the groups regarding tobacco habits. Hence, the confounding effects of tobacco on outcome were nullified.

Past dental visit is an important indicator for the presence of oral diseases, related symptoms and patients' knowledge and belief about dental treatment.[31] The most of the RA and comparison group participants attended the dental clinic although the differences between the groups were not significant.

In earlier studies, duration of RA range from 3.4 months to 17.4 years and the mean duration of disease in this studies were (8.7–17.4) years.[8],[9],[18],[20],[21],[25],[27],[29] The current study is in line with previous studies (8.34 ± 6.47 years).

Dental plaque is the most important local risk factor for gingival bleeding.[29] There was no significant difference with mean number of teeth with gingival bleeding among the RA (20.92 ± 3.13) and comparison group (19.62 ± 5.08). Whereas earlier studies have reported similar mean values for RA group (13.0 ± 10.4–20.1 ± 15.4) and lesser values in comparison group (4.6 ± 5.5–12.3 ± 10.9).[16],[17],[19],[31] Furthermore, similar bleeding score may be inferred that the amount of destruction seen in the RA group could be attributed to other factors, not with only plaque and insufficient oral hygiene.

Studies considering probing depth as indicator of PD have mixed results. Some studies observed significantly higher mean values in participants in RA group than comparison group.[11],[17],[25],[26],[19],[21],[22],[23] whereas, two previous studies found no significant difference.[9],[16]

In the present study, RA participants had significantly higher mean number of teeth with shallow, i.e., 4–5 mm periodontal pocket and deep pocket, i.e., 6 mm or more as compared to comparison group. This finding suggests that underlying systemic components might had an impact on the manifestation of the severity of moderate to advanced periodontitis among RA patients.

Studies considering probing depth as well as CAL [9],[11],[16],[17],[18],[19],[26] and radiographic bone loss [16],[20] have observed significantly higher periodontitis in participants in RA group than comparison group.

In the present study, the prevalence of LOA was significantly higher among the RA group (61%) as compared to comparison group (44%). Moderate-to-severe periodontitis (LOA score = 2–4) was higher among RA group (35%) than comparison group (14%). These findings were in line with one study.[22] Regarding mean number of sextants with LOA, there was significance difference between RA and comparison group.

TMDs have been defined as pathological conditions which produce musculoskeletal pain and dysfunction in the temporomandibular system. These conditions are characterized by a constellation of signs and symptoms including pain associated with jaw function, limited range of mandibular motion, masticatory muscle, and TMJ tenderness on palpation, and TMJ sounds.[8]

Helkimo published an epidemiologic index, with five commonly observed physical signs and symptoms to score what was then called “functional disturbance of the masticatory system.” It was developed specifically as an epidemiologic survey examination for investigating the prevalence of “global” TMDs and the need for treatment.[15],[28]

There was a significant difference between RA and comparison group regarding Impaired Mobility Three out of ten participants in RA group had severe impaired movement. This might be attributed to articular changes in TMJ joint or changes in shape of the coronoid process leading to existing signs of impairment of jaw mobility, reduced mouth opening, and restricted horizontal movement of mandible among patients with RA disease.[15]

Altered function in TMD was due to clicking sound during movement and luxation, locking or laterotrusion <2 mm. The clicking sound raised probably originate in the joints, but the mechanism for locking may be completely different from the mechanism for luxation.[15] There was significant difference between RA and comparison group regarding altered function one out of ten participants in RA group had severe altered function.

Pain is an important symptom for TMD. Literature stated pain on mandibular movement was the strongest predictor of an inflammatory intra-articular milieu which is, indicating an active local inflammation.[6],[8],[16] Painful function of mandible with one or more movement described as TMD, muscle, and TMJ pain was related to sensitivity to pressure on 1–3 places or more places. Two out of ten participants in RA group had severe painful function which was statistically significant.

Pain at rest represents admix of central and peripheral sensitization with endogenous activation of the nociceptive system. Muscle pain is related to muscle of mastication.[6],[8],[29] Significant difference was found between RA and comparison group regarding Muscle pain. One out of four participants in RA group had severe muscle pain.

TMJ pain on movement and chewing represents intra/periarticular mechanical sensitization, palpatory tenderness represents mechanical sensitization from external pressure. Approximately one out of ten participants in RA group had severe TMJ pain which was statistically significant.

Peripheral mechanisms, which may be initiated by excessive loading of the TMJ, cause pain by mechanical stimulation of nociceptors, increased release of neuropeptides and inflammatory mediators and/or local hypoxia. There is increase of inflammatory mediators among RA patients might aggravate the painful condition of TMD.[6],[9] Although painful function in TMD among RA patients are likely to be overshadowed by joint pains elsewhere in the body and most of the RA patients are under NSAID medication,[27],[28] still we found the difference in this study between the group suggest higher severity of TMD condition, irrespective of their medication among RA group.

The clinical dysfunction index considers a functional evaluation of the masticatory system. In accordance with the presence and severity of these clinical symptoms, scores was attained. The individuals were classified into four groups on the basis of the presence of symptoms.[15] Significant difference was observed in relation to TMD between RA and comparison group.

Minor dysfunction in RA group (40%) which was slightly lower than the comparison group (44%). This might be attributed to minor dysfunction that is present in the general population and related to their age, tooth loss, habits, and intra-articular structure. About three-fifth of the study participants (58%) among RA group had moderate-to-severe TMD as compared to one-fifth of the participants in comparison group (22%). Studies that have considered clinical examination and radiographs for assessment of TMD have concluded higher proportion of TMDs (>50%) was in the line of the present study.[27]

The systemic inflammatory activity related to RA is an important factor behind the degree of impact of TMD. In this study, duration of the disease moderately correlated with TMDs (r = 0.649) and weakly correlated with periodontitis (r = 0.308) and correlation was statistically significant. The positive correlation might also suggest that systemic inflammatory mediators' accumulation increase with duration of disease which might play a role in TMD and PD. However, this relation could be attributed due to anti-inflammatory and analgesic drugs, which resolve the symptoms with some extent. Similarly, a possible link between the manifestations of these two chronic inflammatory diseases and remarkable similarities in the pathogenesis of these two conditions at both the cellular and molecular level is suggested in earlier studies. Similar relationships (RA and PD) were reported in some of the previous studies.[17],[19],[26]

The present study demonstrated higher odds (4.8) of TMD and periodontitis (2.16) among RA group than the comparison group. However, there are no studies to compare TMDs among RA patients. Whereas the current study findings are in line with studies reporting similar range of odds for periodontitis among RA patients (1.13–6.09).[2],[20],[23],[24] These findings further evidence that a relationship exists between disease experiences of periodontitis and TMDs in patients with RA. Although it is not suggested as causal relationship, RA group participants were more likely to experience significant TMDs and periodontitis than the comparison group.

Study setting (specialty hospitals) and large sample size can be considered a major strength in the present study in comparison to previous studies. The main limitation of the present study is its cross-sectional nature since data on risk factors and outcome were assessed at the same time which complicates the drawing of causal inferences.

Further investigation into this relationship is necessary, to shed some light on the workings of the inflammatory cells that destroy the bone in both diseases. In particular, longitudinal multicenter studies are necessary to consider confounding factors including stress, nutritional factors and lifestyle and their correlation with periodontitis, TMD, and RA at the same time. Host modulation is key risk factor for the progression of the periodontitis due to RA. Many patients with RA take anti-inflammatory, NSAIDs, and immunosuppressant for their systemic condition. These medications also lead to decrease periodontal inflammation, yet they have significant periodontal destruction. This indicates that before the development of RA symptoms, periodontitis was most likely developing and not detected.

Hence, close cooperation between dentists and rheumatologists is required to improve patient status, and dental consultation should be mandatory when RA first diagnosed. Motivation to maintain oral hygiene with certain modification such as the use of power toothbrush, chlorhexidine mouthwash is recommended among RA patients. Oral health professional needs to instruct the patients with RA to stop the oral habits that adversely affect the TMJ and consult them before any sign and symptoms of TMD.


  Conclusion Top


The prevalence of LOA and TMD was significantly higher among the RA group as compared to comparison group. Significant moderate positive correlation was found between duration of disease and severity of TMD.

Acknowledgment

Special thanks to all study participants and authorities of Rheumatology centers

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.

 
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    Tables

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


This article has been cited by
1 Relationship between rheumatoid arthritis and periodontal disease in Korean adults: Data from the Sixth Korea National Health and Nutrition Examination Survey, 2013 to 2015
Eun Seo Jung,Yoon Young Choi,Kyeong Hee Lee
Journal of Periodontology. 2018;
[Pubmed] | [DOI]



 

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