International Journal of Rheumatic Diseases 2014; 17: 511–518
ORIGINAL ARTICLE
Periodontal disease in Thai patients with rheumatoid arthritis Nuttapong KHANTISOPON,1,2 Worawit LOUTHRENOO,3 Nuntana KASITANON,3 Chate SIVASOMBOON,4 Suparaporn WANGKAEW,3 Supatra SANG-IN,2 Nitaya JOTIKASTHIRA2 and Panwadee BANDHAYA2 1
Department of Dentistry, Samut Sakhon Hospital, Samut Sakhon, 2Department of Restorative Dentistry and Periodontology, Faculty of Dentistry, Chiang Mai University, 3Department of Internal Medicine, Faculty of Medicine, Chiang Mai University, and 4 Department of Radiology, Faculty of Medicine, Chiang Mai University, Chiang Mai, Thailand
Abstract Aim: To evaluate the prevalence and severity of periodontal disease in patients with rheumatoid arthritis (RA) who attended a rheumatology clinic in a university hospital. Methods: All consecutive patients with RA who attended the rheumatology clinic between June 2009 and January 2010 were asked to enroll in this study. All participants answered questionnaires, which included demographic data, medical history, medications used and smoking habits. A full mouth periodontal examination, including gingival index, plaque index, probing pocket depth and clinical attachment level was performed. Only cases that had at least 20 teeth were included in this study. Rheumatoid arthritis parameters, including number of tender and swollen joints, erythrocyte sedimentation rate, the presence of rheumatoid factor (RF), hand radiographs, Disease Activity Index (DAS) and health status using the Thai Health Assessment Questionnaire (HAQ), were determined. The association between RA parameters and periodontal condition was examined. Results: There were 196 participants (87.2% female) with a mean age of 51.7 9.70 years, mean disease duration of 9.62 7.0 years and mean DAS score of 4.64 1.25. Eighty-two per cent were RF-positive. Moderate and severe periodontitis were found in 42% and 57%, respectively. Higher age, male gender, previous or current smoking and high level of plaque score were associated with severe periodontal disease. No differences in RA parameters were found between groups of patients who had moderate and severe periodontitis. Conclusions: We found a high prevalence of periodontitis in Thai patients with RA. However, there was no association between RA parameters and periodontal conditions. Key words: periodontitis, rheumatoid arthritis, risk factor.
INTRODUCTION Periodontal disease is an asymptomatic infectious disease initiated by bacteria, predominantly Gramnegative anaerobic or facultative species, present in den-
Correspondence: Dr. Panwadee Bandhaya, Department of Restorative Dentistry and Periodontology, Faculty of Dentistry, Chiang Mai University, Chiang Mai 50200, Thailand. Email: [email protected]
tal biofilm on tooth root surfaces. Long-term plaque accumulation induces chronic inflammation, which can lead to destruction of the attachment of the periodontal ligament and the adjacent alveolar bone.1 Periodontal disease may be related to a number of various systemic conditions, including diabetes,2 preterm low birth weight,3 coronary heart disease,4 myocardial infarction,5 stroke6 and rheumatoid arthritis (RA).7,8 RA may influence the pathogenesis of periodontitis through its motor and emotional
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impairment.9 Motor impairment may make it more difficult to perform adequate oral hygiene in patients with RA, making them susceptible to plaque accumulation and, consequently, inflammatory periodontal destruction. The salivary flow reduction, or sicca symptoms, which is very common in patients with RA, may increase supragingival plaque formation.10 Although the etiologies of RA and periodontal disease are distinctly separate, a similarity in pathogenesis between these diseases has been reported.11 Both conditions are associated with destruction of connective tissue and bone through an inflammatory process and an immune response.12 Periodontal infection may trigger or potentiate the pathogenesis of RA through bacterial antigens, the presence of inflammatory mediators or immunoglobulins in the serum. Also, periodontopathic bacteria can trigger rheumatic diseases.12–15 Moreover, some studies show common genetic factors among RA and periodontitis.16,17 However, the existence of an association between RA and periodontal disease is still in question. Several reports have shown that patients with RA have an increased prevalence and severity of periodontal disease. A study from Australia reported 62.5% of RA patients had advanced forms of periodontitis.8 Pischon et al. reported high mean clinical attachment level (CAL) in RA patients compared to non-RA patients in Germany.19 A pilot study in the USA by Dissick et al. found 51% of RA patients had moderate to severe forms of periodontitis.20 Also, 70% of RA patients in Indonesia and 40% of those in Taiwan had periodontitis.21,22 Yet, other studies did not find higher prevalence or severity of periodontal status between patients with RA and non-RA controls.23,24 Studies of association between RA and periodontitis have been performed in many populations with different genetic backgrounds, including populations in Australia,18 America,25 Europe26 and Japan.24 There has been only limited study in South East Asia.21 This study was performed to evaluate the prevalence and severity of periodontal disease in Thai patients with RA and to identify factors that might affect the extent of periodontal disease in this population.
MATERIALS AND METHODS This study was approved by the Human Experimentation Committees of the Faculty of Dentistry and the Faculty of Medicine, Chiang Mai University (Protocol number 10/2009). Written informed consent was obtained from all subjects prior to their enrollment.
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Study population All patients with RA who attended the outpatient rheumatology clinic at the Chiang Mai University Hospital, between June 2009 and January 2010 were asked to participate in this cross-sectional study. The diagnosis of RA followed the 1987 American Rheumatism Association (ARA) revised criteria for the classification of rheumatoid arthritis.27 Only those who had at least 20 teeth present, excluding the third molars, were included in the study. Patients were excluded if they were pregnant, lactating or had systemic conditions that could affect the progression of periodontal disease, such as uncontrolled diabetes mellitus, severe hypertension, severe renal insufficiency or malignancies and so on. In addition, subjects who had a history of taking antibiotics during the previous 3 months were excluded.
Questionaires All participants answered medical and dental questionnaires that requested information on age, sex, sociodemographic characteristics, medical history, use of medication, smoking status and oral hygiene habits.
Rheumatoid arthritis clinical measurement A complete history, physical examination and the medication used for RA were recorded. The activity of RA was determined by Disease Activity Score (DAS28).28 This disease activity index includes a 28 tender and swollen joint count, the erythrocyte sedimentation rate (ESR, mm/h) and the patients’ global assessment of health (using a visual analog scale [VAS] of 0–10). The DAS28 score was performed by well-trained, experienced rheumatologists (WL, NK, SW). A Thai version of the Health Assessment Questionaire (Thai HAQ score) was used to evaluate patient performance regarding daily living.29 Hand HAQ was the sub-score of Thai HAQ score which included only the performance of hand function on daily living, dressing, eating, grip, some instruments and activities which need help. Radiographic damage indices, including joint erosion scores and joint space narrowing scores were assessed according to a modified Sharp/van der Heijde method, and was read by CS, a radiologist who was blinded to the clinical and periodontal features.30 Only hand radiographs were used in this study. Stimulated whole saliva collection (SWSC) was measured for the diagnosis of xerostomia,31 in which a salivary flow rate of less than 0.7 mL/min was considered to be indicative of xerostomia.32 The average income of the Thai population at the time of study was 20 000 Baht/month according to the National Statistical Office (2009).33
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The currency exchange rate during the study period was 33 Baht/US dollar.
Periodontal clinical measurements All patients received a full mouth periodontal examination by one experienced periodontist (NK). Four periodontal variables were determined. Oral hygiene status was evaluated using the plaque index (PI) of Silness and Loe.34 The gingival index (GI) was assessed using the Gingival Index of Loe.35 Each tooth present was examined for gingival recession, periodontal pocket depth and clinical attachment level, in millimeters, at six sites per tooth, using a manual periodontal probe (PCP-UNC 15; Hu-Friedy, Chicago, IL, USA) and the readings were recorded to the nearest 1 mm. Gingival recession was defined as the distance from the cemento-enamel junction (CEJ) to the free gingival margin. Probing depth (PD) was defined as the distance from the free gingival margin to the bottom of the sulcus or periodontal pocket. Clinical attachment level (CAL) was defined as the distance from the CEJ to the bottom of the sulcus or periodontal pocket, and was calculated as the sum of PD and gingival recession measurements. The periodontal status of this population was classified according to the CDC-AAP case definitions36 as follows: mild periodontitis = patients who had ≥ 2 interproximal sites with CAL ≥ 3 mm, and ≥2 interproximal sites with PD ≥ 4 mm (not on the same tooth) or one site with PD ≥ 5 mm; moderate periodontitis = ≥ 2 interproximal sites with CAL ≥ 4 mm (not on the same tooth), or ≥ 2 interproximal sites with PD ≥ 5 mm (not on the same tooth); severe periodontitis = ≥ 2 interproximal sites with CAL ≥ 6 mm (not on the same tooth) and ≥ 1 interproximal site with PD ≥ 5 mm. The examination also included recording the number of teeth present. The values for the weighted Kappa test for the PD and CAL were 0.97 and 1.00, respectively.
Statistical analysis Statistical analysis and data management were performed using the Statistical Package for the Social Sciences, version 17.0 (SPSS Inc., Chicago, IL, USA). The level of statistical significance was set at 0.05. The categorical variables were described as frequency distributions or percentages, and the continuous variables were described as means standard deviations (SD). The association between gender, educational level (primary school or higher than primary school), income (< 20 000 or ≥20 000 Baht), smoking status (none or former/current smoker), plaque index, Thai
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HAQ score, HAQ hand score, salivary flow rate (< 0.70 or >0.70 mL/min), DAS 28 ESR, mean joint erosion score, mean joint space narrowing score, mean total joint erosion and joint space narrowing score and periodontal disease severity, were evaluated using the chi-square or Fisher’s Exact test for discrete variables and the t-test or Mann–Whitney U-test for continuous variables. In order to compare periodontal status of this group of RA patients with the 6th Thailand National Oral Health Survey in the year 2007, we also classified periodontal status according to CPI index and calculated for age–sex adjustment of the Thai population.
RESULTS Two hundred and two patients agreed to participate in the study. Six patients were excluded because of incomplete data; therefore, only 196 patients who had complete data were included in this study. The sociodemograhpic characteristics of the patients are shown in Table 1. Eighty-seven percent of the patients were female. Ninety percent of the patients had incomes that were lower than the Thai average income per household per month (20 903 Baht). Sixty-two percent had a primary school education level. Seventyeight percent had never smoked. Among common co-morbidities, there was hypertension in 62 (30.69%) cases, dyslipidemia in 69 (34.16%), diabetes mellitus in six (2.97%) and chronic kidney disease in five (2.47%). Of 39 patients who had bone density measurements, 23 (58.97%) had osteoporosis and nine (23.08%) had osteopenia. Periodontal findings are shown in Table 1. Mean clinical attachment level was 3.35 0.91 mm. The level of gingival inflammation in this population was low (mean GI index = 0.82 0.46) and oral hygiene was fair (mean PI = 1.21 0.53). Sixty-four percent of the patients had periodontal treatment in the past and 42% had been instructed in the performance of self-care oral hygiene. None had periodontal treatment during the study period. The duration range of RA was 1–32 years (mean 9.62 7.00). Rheumatoid factor (RF) was positive in 82.1% of cases. The range of DAS28 scores was 1.70– 8.56, in which their disease activity was classified as remission, mild, moderate and severe or very active, according to DAS28 criteria of 4.1%, 9.2%, 51.0% and 35.7%, respectively. Despite a majority of the patients having moderate to severe active RA, more than 90% of them had a relatively low Thai HAQ score (mean 0.79 0.68). As only the upper extremity is used for
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Table 1 Socio-demographic, periodontal and medical characteristics of study patients with RA Variables Female n (%) Age (mean SD) Household income/month < 20 000 Baht n (%) Educational level Primary school n (%) Secondary school n (%) University n (%) Smoking status Non-smokers n (%) Periodontal status Remaining teeth (mean SD) Probing depth (mm, mean SD) Clinical attachment level (mm, mean SD) Plaque Index (mean SD) Previous periodontal treatment n (%) Previous oral hygiene instructions n (%) RA status Duration (years, mean SD) RF+ n (%) ESR (mm/h, mean SD) DAS28 (mean SD) Thai HAQ score (mean SD) Upper extremity HAQ score (mean SD) Mean joint erosion score† (mean SD) Mean joint space narrowing score† (mean SD) Total joint erosion and joint space narrowing† (mean SD) Xerostomia n (%) Medications Methotrexate n (%) Prednisolone n (%) Diclofenac n (%) Mono-DMARDs n (%) Combined DMARDs n (%)
171 (87.2) 51.70 9.70 179 (91.3) 122 (62.2) 45 (23) 29 (14.8) 153 (78.1) 25.84 2.28 2.74 0.53 3.35 0.91 1.21 0.53 115 (63.8) 82 (41.8)
9.62 7.00 161 (82.1) 45.76 25.69 4.64 1.25 0.79 0.68 0.66 0.68 36.36 10.41
DISCUSSION
39.92 24.90
In this study, we found a high mean clinical attachment level in this group of Thai patients with RA. According to the CDC-AAP case definitions,36 the periodontal status of this group of patients was classified as moderate and severe periodontits. Only one patient had no periodontitis. This finding was in line with those of previous studies in other countries where a high prevalence of periodontitis in patients with RA was identified (51–70%).8,20,21 However, the prevalence and severity of periodontitis in this study was higher than in others.20,21,37 The reason for such a very high prevalence and severity of periodontal disease in our patients was not clear, but it might be related to the fact that this patient group had a greater severity of RA than patients in other studies appeared to have (86.7% had moderate
76.28 52.69 24 (12.2) 163 (83.2) 111 (56.6) 80 (40.8) 104 (53.1) 78 (39.8)
†Number count from hand radiograph only; RA, rheumatoid arthritis; RF, rheumatoid factor; ESR, erythrocyte sedimentation rate; DAS28, Disease Activity Score of 28 joints; HAQ, Health Assessment Quenstionnaire; DMARDs, disease-modifying antirheumatic drugs.
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dental hygiene care, we therefore calculated only the HAQ score of the upper extremity for analysis. The mean upper extremity HAQ hand score was 0.66 0.68, and 9.7% had upper extremity HAQ >2. The mean salivary flow was 1.44 0.67 mL/min and 12% of patients with RA were classified as having xerostomia. According to the Sharp/van de Heijde score, the patients with RA had a mean joint erosion score, mean joint space narrowing score and mean total joint erosion and joint space narrowing score of 36.36 10.41, 39.92 24.90 and 76.28 52.69, respectively. All patients with RA were treated with one or more medications; 83.2% used methotrexate, 56.6% used prednisolone and 53.1% used mono-disease-modifying antirheumatic drugs. The periodontal status of this population was classified as moderate to severe periodontitis, according to the CDC-AAP case definitions. Only one patient had no periodontitis. The association between sociodemographic characteristics, RA disease characteristics and periodontal parameters between patients who had moderate periodontitis and severe periodontitis is shown in Table 2. Age, male gender, smoking history, number of remaining teeth, plaque index and CAL were significantly different between the two groups of patients. There was no difference in RA variables between patients who had moderate and severe periodontitis. When we used CPI index, 42.6% of the population in the age group 35–44 years had CPI = 3 and 30.1% had CPI = 4. In the age group 60–74 years, 30.8% had CPI = 3 and 69.2% had CPI = 4 (Table 3).
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Table 2 Characteristics of RA and periodontal parameters according to periodontal status
Variables
Male* Age (years)* Household Income < 20 000 Baht/ month Primary school Former/current smokers* Remaining teeth* Plaque index** Mean CAL** Duration of RA (years) DAS28 >3.2 Thai HAQ score >2 Upper extremity; HAQ score >2 Mean joint erosion score Mean joint space narrowing score Mean joint erosion and joint space narrowing score Xerostomia
Moderate periodontitis (n = 83)
Severe periodontitis (n = 112)
5 (6%) 49.48 10.23 75 (90.4%)
19 (17%) 53.37 9.02 103 (92%)
46 (55.4%) 8 (9.6%) 26.34 1.02 2.76 10.00
1.82 0.47 0.45 7.25
75 (67.0%) 34 (30.4%) 25.50 1.37 3.79 9.31
2.51 0.53 0.92 6.85
Pvalue† 0.021 0.006 0.695
0.101 0.001 0.044 < 0.001 < 0.001 0.500
69 (83.1%) 7 (8.4%) 6 (7.2%)
100 (89.3%) 12 (10.7%) 9 (8.0%)
0.211 0.595 0.834
32.80 27.90
39.00 32.15
0.161
37.17 23.41
42.09 25.93
0.174
69.96 48.44
81.09 55.59
0.146
8 (9.6%)
16 (13.9%)
0.329
*P < 0.05, **P < 0.001, †P-values are based on the t-test or Mann–Whitney U-test for continuous data or v2 test for frequency data.
Table 3 Periodontal status of the Thai population in the 6th Thailand National Oral Health Survey (2007) compared to the periodontal status of patients with RA according to CPI index Age group
35–44 60–74
CPI = 3
CPI = 4
Thailand national survey (%)
RA (%)
Thailand national survey (%)
RA (%)
22.1 15.4
42.6 30.8
15.5 68.8
50.1 69.2
to severe active RA and the duration, 9.62 7.00 years, was longer).20,21,37 Although previous reports could not find an association between RA disease severity and periodontitis severity,19,20 the most recent study by Smit et al.37 in 2012 showed a significant finding of severe periodontitis in patients with higher DAS28 scores than in those with no or moderate periodontitis. K€asser et al.38 showed that patients with long-standing, active RA had increased CAL by 173%.
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An important factor that might influence prevalence of periodontitis was the criteria used to classify periodontal disease. There are many periodontal case definitions used in periodontal research.39 The different case definitions have a high impact on prevalence of periodontitis and produce different associations in risk factors of periodontitis.40,41 Some studies used dental radiographs8 or in combination with bleeding on probing and tooth mobility.20 A study in Taiwan, in which a history of periodontal treatment and cumulative costs of the periodontitis-related visit were used to classify peridontitis cases, found a prevalence of periodontitis of 40%.22 However, the use of history and cumulative costs of periodontal treatment raises the issue of accuracy of the diagnostic criteria used to classify periodontitis in their paper. In this study, we classified prevalence and severity of periodontal disease according to CDC-AAP case definitions,36 which was the same criteria used in a study of Indonesian populations.21 These criteria used CAL and PD to determine periodontitis cases. The advantage of using CAL was to measure
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cumulative periodontal destruction in the past, while using only PD may reflect the damage of supporting structure.42 Moreover, we examined all teeth present in the mouth which could reduce a chance of underestimating periodontitis cases compared to partial mouth records in both prevalence and severity of this disease.43 Taken together, the high prevalence of periodontitis cases in our study may reflect the real situation of periodontal disease in our study group. The previous report from the 6th Thailand National Oral Health Survey in the year 2007 found a high prevalence of periodontitis in the Thai general population.44 However, in that study, periodontitis was classified using the Community Periodontal Index (CPI) score, but only PD was reported, which may underestimate prevalence of periodontitis in a high-age population group.45 However, when we modified our data according to the CPI index, we still found that our patients with RA had higher percentages of periodontitis than did the patients in the 6th Thailand National Oral Health Survey (Table 3). These data indicate that the prevalence of periodontitis in Thai patients with RA is high. When we compared RA clinical parameters and periodontal parameters between groups of patients with moderate and severe peridontitis, the result showed that only plaque level, mean CAL, age, male gender and smoking status showed a statistically significant difference. Oral hygiene was a strong risk indicator for periodontitis in the general population.46 However, a study by Pischon et al.19 found that oral hygiene may only partially account for the development of periodontitis in patients with RA. In this study, the average oral hygine level of the patients was fair, and it was in concordance with the upper extremity of the HAQ score, as only 9.7% of the patients had upper extremity HAQ scores >2. Therefore, the ability of the patients in this study group to perform oral hygiene practices might not be impaired by their RA disease severity. Thus, oral hygiene might not play an important role in developing periodontitis in this patient group. Age and male gender have been found as risk indicators for periodontitis.47 Therefore, it was no surprise that those who had severe periodontitis had a higher average age than those with moderate peridontitis. Smoking is also a powerful risk factor for periodontitis47 and it has been shown to be a risk factor for RA development and severity.48 Our results showed a strong association between former/ current smokers and the severe form of peridontitis. This association agreed with other studies, which found higher prevalence and severity of periodontitis in smokers, in a dose-dependent manner.47 Nevertheless,
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it should be noted that most patients in this study were non-smokers. Taken all together, age, oral hygiene and smoking were the only contributing factors for developing the severe form of peridontitis in this population. The factors that might contribute to developing periodontitis in this study group needs to be further elucidated. Our study is the first report of periodontal status in a group of patients with RA in Thailand. The information from our study might merit further investigation for advanced knowledge regarding the relationship between RA disease and periodontitis. Our study population was quite large, compared to some other previous reports.19,37 To minimize under- or over-estimation, we included only subjects who had 20 teeth or more (excluding third molars) and all presenting teeth were examined. Therefore, the periodontal conditions in our patients with RA represented the true status of the study population. Some of the previous studies had reported the numbers of teeth lost, but the reasons for the loss were not mentioned.18,19 In fact, the major causes of tooth loss in the general population are dental caries and periodontal disease.49 The only important reason for tooth loss in these studies was from periodontal disease, which might influence the interpretation of the results. Our study had some limitations. It was a cross-sectional study and did not have a control group; so we could not compare potential risk factors for having periodontitis in this study population. Another limitation was the lack of intra-oral radiographs in this study, resulting in an inability to measure the level of bone loss and compare it with periodontal clinical parameters. However, in this study, we measured the clinical attachment level, which has been shown to have a relationship with bone loss.50 Thus, the periodontal status in our study may represent the level of periodontal destruction in a Thai population with RA. Lastly, we did not have a chance to measure anti-citrullinated peptide antibodies (ACPA) in our RA patients, as by the time of the study, the ACPA test was very expensive and was not routinely available at our hospital. Future study of the association of ACPA and periodontitis might be of interest.
CONCLUSIONS In this study, we found that Thai patients with RA had a high prevalence of moderate or severe periodontal disease. Increasing age, male gender, previous or current smoking and a high plaque score were associated with severity of periodontal disease. The RA clinical
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parameters, the medication used and the upper extremity HAQ score showed no association with moderate or severe periodontal disease in this population.
ACKNOWLEDGEMENTS The authors thank Mrs. Woraporn Sukittawut, B.Sc. and Rheumatology staff for their secretarial assistance. This study was supported by a graduate thesis grant, Faculty of Dentistry, Chiang Mai University. The authors also thank Dr. M. Kevin O’Carroll, Professor Emeritus of the University of Mississippi School of Dentistry, USA and Faculty Consultant at Chiang Mai University Faculty of Dentistry, Thailand, for his critical reading of this manuscript.
CONFLICT OF INTEREST All authors declare no conflict of interest.
REFERENCES 1 Page RC, Offenbacher S, Schroeder HE, Seymour GJ, Kornman KS (1997) Advances in the pathogenesis of periodontitis: summary of developments, clinical implications and future directions. Periodontol 2000 14, 216–48. 2 Mealey BL, Oates TW (2006) Diabetes mellitus and periodontal diseases. J Periodontol 77, 1289–303. 3 Offenbacher S, Katz V, Fertik G et al. (1996) Periodontal infection as a possible risk factor for preterm low birth weight. J Periodontol 67, 1103–13. 4 Beck J, Garcia R, Heiss G, Vokonas PS, Offenbacher S (1996) Periodontal disease and cardiovascular disease. J Periodontol 67, 1123–37. 5 Rutger Persson G, Ohlsson O, Pettersson T, Renvert S (2003) Chronic periodontitis, a significant relationship with acute myocardial infarction. Eur Heart J 24, 2108–15. 6 Grau AJ, Becher H, Ziegler CM et al. (2004) Periodontal disease as a risk factor for ischemic stroke. Stroke 35, 496– 501. 7 Al-Shammari KF, Al-Khabbaz AK, Al-Ansari JM, Neiva R, Wang HL (2005) Risk indicators for tooth loss due to periodontal disease. J Periodontol 76, 1910–8. 8 Mercado F, Marshall RI, Klestov AC, Bartold PM (2000) Is there a relationship between rheumatoid arthritis and periodontal disease? J Clin Periodontol 27, 267–72. 9 Persson LO, Berglund K, Sahlberg D (1999) Psychological factors in chronic rheumatic diseases–a review. The case of rheumatoid arthritis, current research and some problems. Scand J Rheumatol 28, 137–44. 10 Antoniazzi RP, Miranda LA, Zanatta FB et al. (2009) Periodontal conditions of individuals with Sjogren’s syndrome. J Periodontol 80, 429–35.
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11 Berthelot JM, Le Goff B (2010) Rheumatoid arthritis and periodontal disease. Joint Bone Spine 77, 537–41. 12 Rosenstein ED, Greenwald RA, Kushner LJ, Weissmann G (2004) Hypothesis: the humoral immune response to oral bacteria provides a stimulus for the development of rheumatoid arthritis. Inflammation 28, 311–8. 13 Bartold PM, Marino V, Cantley M, Haynes DR (2010) Effect of Porphyromonas gingivalis-induced inflammation on the development of rheumatoid arthritis. J Clin Periodontol 37, 405–11. 14 Martinez-Martinez RE, Abud-Mendoza C, Patino-Marin N, Rizo-Rodriguez JC, Little JW, Loyola-Rodriguez JP (2009) Detection of periodontal bacterial DNA in serum and synovial fluid in refractory rheumatoid arthritis patients. J Clin Periodontol 36, 1004–10. 15 Nesse W, Westra J, van der Wal JE et al. (2012) The periodontium of periodontitis patients contains citrullinated proteins which may play a role in ACPA (anti-citrullinated protein antibody) formation. J Clin Periodontol 39, 599–607. 16 Bonfil JJ, Dillier FL, Mercier P et al. (1999) A “case control” study on the role of HLA DR4 in severe periodontitis and rapidly progressive periodontitis. Identification of types and subtypes using molecular biology (PCR.SSO). J Clin Periodontol 26, 77–84. 17 Ishida K, Kobayashi T, Ito S et al. (2012) Interleukin-6 gene promoter methylation in rheumatoid arthritis and chronic periodontitis. J Periodontol 83, 917–25. 18 Mercado FB, Marshall RI, Klestov AC, Bartold PM (2001) Relationship between rheumatoid arthritis and periodontitis. J Periodontol 72, 779–87. 19 Pischon N, Pischon T, Kroger J et al. (2008) Association among rheumatoid arthritis, oral hygiene, and periodontitis. J Periodontol 79, 979–86. 20 Dissick A, Redman RS, Jones M et al. (2010) Association of periodontitis with rheumatoid arthritis: a pilot study. J Periodontol 81, 223–30. 21 Susanto H, Nesse W, Kertia N et al. (2013) Prevalence and severity of periodontitis in indonesian patients with rheumatoid arthritis. J Periodontol 84, 1067–74. 22 Chen HH, Huang N, Chen YM et al. (2013) Association between a history of periodontitis and the risk of rheumatoid arthritis: a nationwide, population-based, case-control study. Ann Rheum Dis 72, 1206–11. 23 Sjostrom L, Laurell L, Hugoson A, Hakansson JP (1989) Periodontal conditions in adults with rheumatoid arthritis. Community Dent Oral Epidemiol 17, 234–6. 24 Kobayashi T, Murasawa A, Komatsu Y et al. (2010) Serum cytokine and periodontal profiles in relation to disease activity of rheumatoid arthritis in Japanese adults. J Periodontol 81, 650–7. 25 de Pablo P, Dietrich T, McAlindon TE (2008) Association of periodontal disease and tooth loss with rheumatoid arthritis in the US population. J Rheumatol 35, 70–6. 26 Havemose-Poulsen A, Westergaard J, Stoltze K et al. (2006) Periodontal and hematological characteristics
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27
28
29
30
31
32
33
34
35 36
37
38
associated with aggressive periodontitis, juvenile idiopathic arthritis, and rheumatoid arthritis. J Periodontol 77, 280–8. Arnett FC, Edworthy SM, Bloch DA et al. (1988) The American Rheumatism Association 1987 revised criteria for the classification of rheumatoid arthritis. Arthritis Rheum 31, 315–24. Smolen JS, Breedveld FC, Eberl G et al. (1995) Validity and reliability of the twenty-eight-joint count for the assessment of rheumatoid arthritis activity. Arthritis Rheum 38, 38–43. Osiri M, Deesomchok U, Tugwell P (2001) Evaluation of functional ability of Thai patients with rheumatoid arthritis by the use of a Thai version of the Health Assessment Questionnaire. Rheumatology (Oxford) 40, 555–8. van der Heijde D (2000) How to read radiographs according to the Sharp/van der Heijde method. J Rheumatol 27, 261–3. Jensen JL, Karatsaidis A, Brodin P (1998) Salivary secretion: stimulatory effects of chewing-gum versus paraffin tablets. Eur J Oral Sci 106, 892–6. Malmstrom MJ, Segerberg-Konttinen M, Tuominen TS et al. (1988) Xerostomia due to Sjogren’s syndrome. Diagnostic criteria, treatment and outlines for a continuous dental care programme and an open trial with Sulfarlem. Scand J Rheumatol 17, 77–86. The Household Socio-Economic Survey (2009) (Internet). National Statistical Office, Bangkok. [Cited 6 Apr 2013.] Available from: http://www.nso.go.th. Silness J, Loe H (1964) Periodontal disease in pregnancy. Ii. Correlation between oral hygiene and periodontal condition. Acta Odontol Scand 22, 121–35. Loe H, Silness J (1963) Periodontal disease in pregnancy I. Prevalence and severity. Acta Odontol Scand 21, 533–51. Eke PI, Page RC, Wei L, Thornton-Evans G, Genco RJ (2012) Update of the case definitions for population-based surveillance of periodontitis. J Periodontol 83, 1449–54. Smit MD, Westra J, Vissink A, Doornbos-van der Meer B, Brouwer E, van Winkelhoff AJ (2012) Periodontitis in established rheumatoid arthritis patients: a cross-sectional clinical, microbiological and serological study. Arthritis Res Ther 14, R222. K€asser UR, Gleissner C, Dehne F, Michel A, WillershausenZonnchen B, Bolten WW (1997) Risk for periodontal disease in patients with longstanding rheumatoid arthritis. Arthritis Rheum 40, 2248–51.
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39 Savage A, Eaton KA, Moles DR, Needleman I (2009) A systematic review of definitions of periodontitis and methods that have been used to identify this disease. J Clin Periodontol 36, 458–67. 40 Costa FO, Guimaraes AN, Cota LO et al. (2009) Impact of different periodontitis case definitions on periodontal research. J Oral Sci 51, 199–206. 41 Kassab P, Colombier ML, Kaminski M, Lelong N, Sixou M, Nabet C (2011) Impact of periodontitis definition in epidemiological research. Results from the EPIPAP study in postpartum women. Eur J Oral Sci 119, 156–62. 42 Beltran-Aguilar ED, Eke PI, Thornton-Evans G, Petersen PE (2012) Recording and surveillance systems for periodontal diseases. Periodontol 2000 60, 40–53. 43 Kingman A, Susin C, Albandar JM (2008) Effect of partial recording protocols on severity estimates of periodontal disease. J Clin Periodontol 35, 659–67. 44 The 6th Thailand National Oral Health Survey (2007) (Internet). Department of Health, Ministry of Health, Bangkok. [Cited 10 Feb 2014.] Available from: http:// dental.anamai.moph.go.th/oral health/PR/E-book/Survey/ survey6th.pdf. 45 Baelum V, Manji F, Wanzala P, Fejerskov O (1995) Relationship between CPITN and periodontal attachment loss findings in an adult population. J Clin Periodontol 22, 146– 52. 46 Tanner AC, Kent R Jr, Van Dyke T, Sonis ST, Murray LA (2005) Clinical and other risk indicators for early periodontitis in adults. J Periodontol 76, 573–81. 47 Torrungruang K, Nisapakultorn K, Sutdhibhisal S et al. (2005) The effect of cigarette smoking on the severity of periodontal disease among older Thai adults. J Periodontol 76, 566–72. 48 Navarro-Compan V, Melguizo-Madrid E, Hernandez-Cruz B et al. (2013) Interaction between oxidative stress and smoking is associated with an increased risk of rheumatoid arthritis: a case-control study. Rheumatology (Oxford) 52, 487–93. 49 Beltran-Aguilar ED, Beltran-Neira RJ (2004) Oral diseases and conditions throughout the lifespan. I. Diseases and conditions directly associated with tooth loss. Gen Dent 52, 21–7. 50 Goodson JM, Haffajee AD, Socransky SS (1984) The relationship between attachment level loss and alveolar bone loss. J Clin Periodontol 11, 348–59.
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ORIGINAL ARTICLE
Periodontal disease in Thai patients with rheumatoid arthritis Nuttapong KHANTISOPON,1,2 Worawit LOUTHRENOO,3 Nuntana KASITANON,3 Chate SIVASOMBOON,4 Suparaporn WANGKAEW,3 Supatra SANG-IN,2 Nitaya JOTIKASTHIRA2 and Panwadee BANDHAYA2 1
Department of Dentistry, Samut Sakhon Hospital, Samut Sakhon, 2Department of Restorative Dentistry and Periodontology, Faculty of Dentistry, Chiang Mai University, 3Department of Internal Medicine, Faculty of Medicine, Chiang Mai University, and 4 Department of Radiology, Faculty of Medicine, Chiang Mai University, Chiang Mai, Thailand
Abstract Aim: To evaluate the prevalence and severity of periodontal disease in patients with rheumatoid arthritis (RA) who attended a rheumatology clinic in a university hospital. Methods: All consecutive patients with RA who attended the rheumatology clinic between June 2009 and January 2010 were asked to enroll in this study. All participants answered questionnaires, which included demographic data, medical history, medications used and smoking habits. A full mouth periodontal examination, including gingival index, plaque index, probing pocket depth and clinical attachment level was performed. Only cases that had at least 20 teeth were included in this study. Rheumatoid arthritis parameters, including number of tender and swollen joints, erythrocyte sedimentation rate, the presence of rheumatoid factor (RF), hand radiographs, Disease Activity Index (DAS) and health status using the Thai Health Assessment Questionnaire (HAQ), were determined. The association between RA parameters and periodontal condition was examined. Results: There were 196 participants (87.2% female) with a mean age of 51.7 9.70 years, mean disease duration of 9.62 7.0 years and mean DAS score of 4.64 1.25. Eighty-two per cent were RF-positive. Moderate and severe periodontitis were found in 42% and 57%, respectively. Higher age, male gender, previous or current smoking and high level of plaque score were associated with severe periodontal disease. No differences in RA parameters were found between groups of patients who had moderate and severe periodontitis. Conclusions: We found a high prevalence of periodontitis in Thai patients with RA. However, there was no association between RA parameters and periodontal conditions. Key words: periodontitis, rheumatoid arthritis, risk factor.
INTRODUCTION Periodontal disease is an asymptomatic infectious disease initiated by bacteria, predominantly Gramnegative anaerobic or facultative species, present in den-
Correspondence: Dr. Panwadee Bandhaya, Department of Restorative Dentistry and Periodontology, Faculty of Dentistry, Chiang Mai University, Chiang Mai 50200, Thailand. Email: [email protected]
tal biofilm on tooth root surfaces. Long-term plaque accumulation induces chronic inflammation, which can lead to destruction of the attachment of the periodontal ligament and the adjacent alveolar bone.1 Periodontal disease may be related to a number of various systemic conditions, including diabetes,2 preterm low birth weight,3 coronary heart disease,4 myocardial infarction,5 stroke6 and rheumatoid arthritis (RA).7,8 RA may influence the pathogenesis of periodontitis through its motor and emotional
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impairment.9 Motor impairment may make it more difficult to perform adequate oral hygiene in patients with RA, making them susceptible to plaque accumulation and, consequently, inflammatory periodontal destruction. The salivary flow reduction, or sicca symptoms, which is very common in patients with RA, may increase supragingival plaque formation.10 Although the etiologies of RA and periodontal disease are distinctly separate, a similarity in pathogenesis between these diseases has been reported.11 Both conditions are associated with destruction of connective tissue and bone through an inflammatory process and an immune response.12 Periodontal infection may trigger or potentiate the pathogenesis of RA through bacterial antigens, the presence of inflammatory mediators or immunoglobulins in the serum. Also, periodontopathic bacteria can trigger rheumatic diseases.12–15 Moreover, some studies show common genetic factors among RA and periodontitis.16,17 However, the existence of an association between RA and periodontal disease is still in question. Several reports have shown that patients with RA have an increased prevalence and severity of periodontal disease. A study from Australia reported 62.5% of RA patients had advanced forms of periodontitis.8 Pischon et al. reported high mean clinical attachment level (CAL) in RA patients compared to non-RA patients in Germany.19 A pilot study in the USA by Dissick et al. found 51% of RA patients had moderate to severe forms of periodontitis.20 Also, 70% of RA patients in Indonesia and 40% of those in Taiwan had periodontitis.21,22 Yet, other studies did not find higher prevalence or severity of periodontal status between patients with RA and non-RA controls.23,24 Studies of association between RA and periodontitis have been performed in many populations with different genetic backgrounds, including populations in Australia,18 America,25 Europe26 and Japan.24 There has been only limited study in South East Asia.21 This study was performed to evaluate the prevalence and severity of periodontal disease in Thai patients with RA and to identify factors that might affect the extent of periodontal disease in this population.
MATERIALS AND METHODS This study was approved by the Human Experimentation Committees of the Faculty of Dentistry and the Faculty of Medicine, Chiang Mai University (Protocol number 10/2009). Written informed consent was obtained from all subjects prior to their enrollment.
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Study population All patients with RA who attended the outpatient rheumatology clinic at the Chiang Mai University Hospital, between June 2009 and January 2010 were asked to participate in this cross-sectional study. The diagnosis of RA followed the 1987 American Rheumatism Association (ARA) revised criteria for the classification of rheumatoid arthritis.27 Only those who had at least 20 teeth present, excluding the third molars, were included in the study. Patients were excluded if they were pregnant, lactating or had systemic conditions that could affect the progression of periodontal disease, such as uncontrolled diabetes mellitus, severe hypertension, severe renal insufficiency or malignancies and so on. In addition, subjects who had a history of taking antibiotics during the previous 3 months were excluded.
Questionaires All participants answered medical and dental questionnaires that requested information on age, sex, sociodemographic characteristics, medical history, use of medication, smoking status and oral hygiene habits.
Rheumatoid arthritis clinical measurement A complete history, physical examination and the medication used for RA were recorded. The activity of RA was determined by Disease Activity Score (DAS28).28 This disease activity index includes a 28 tender and swollen joint count, the erythrocyte sedimentation rate (ESR, mm/h) and the patients’ global assessment of health (using a visual analog scale [VAS] of 0–10). The DAS28 score was performed by well-trained, experienced rheumatologists (WL, NK, SW). A Thai version of the Health Assessment Questionaire (Thai HAQ score) was used to evaluate patient performance regarding daily living.29 Hand HAQ was the sub-score of Thai HAQ score which included only the performance of hand function on daily living, dressing, eating, grip, some instruments and activities which need help. Radiographic damage indices, including joint erosion scores and joint space narrowing scores were assessed according to a modified Sharp/van der Heijde method, and was read by CS, a radiologist who was blinded to the clinical and periodontal features.30 Only hand radiographs were used in this study. Stimulated whole saliva collection (SWSC) was measured for the diagnosis of xerostomia,31 in which a salivary flow rate of less than 0.7 mL/min was considered to be indicative of xerostomia.32 The average income of the Thai population at the time of study was 20 000 Baht/month according to the National Statistical Office (2009).33
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The currency exchange rate during the study period was 33 Baht/US dollar.
Periodontal clinical measurements All patients received a full mouth periodontal examination by one experienced periodontist (NK). Four periodontal variables were determined. Oral hygiene status was evaluated using the plaque index (PI) of Silness and Loe.34 The gingival index (GI) was assessed using the Gingival Index of Loe.35 Each tooth present was examined for gingival recession, periodontal pocket depth and clinical attachment level, in millimeters, at six sites per tooth, using a manual periodontal probe (PCP-UNC 15; Hu-Friedy, Chicago, IL, USA) and the readings were recorded to the nearest 1 mm. Gingival recession was defined as the distance from the cemento-enamel junction (CEJ) to the free gingival margin. Probing depth (PD) was defined as the distance from the free gingival margin to the bottom of the sulcus or periodontal pocket. Clinical attachment level (CAL) was defined as the distance from the CEJ to the bottom of the sulcus or periodontal pocket, and was calculated as the sum of PD and gingival recession measurements. The periodontal status of this population was classified according to the CDC-AAP case definitions36 as follows: mild periodontitis = patients who had ≥ 2 interproximal sites with CAL ≥ 3 mm, and ≥2 interproximal sites with PD ≥ 4 mm (not on the same tooth) or one site with PD ≥ 5 mm; moderate periodontitis = ≥ 2 interproximal sites with CAL ≥ 4 mm (not on the same tooth), or ≥ 2 interproximal sites with PD ≥ 5 mm (not on the same tooth); severe periodontitis = ≥ 2 interproximal sites with CAL ≥ 6 mm (not on the same tooth) and ≥ 1 interproximal site with PD ≥ 5 mm. The examination also included recording the number of teeth present. The values for the weighted Kappa test for the PD and CAL were 0.97 and 1.00, respectively.
Statistical analysis Statistical analysis and data management were performed using the Statistical Package for the Social Sciences, version 17.0 (SPSS Inc., Chicago, IL, USA). The level of statistical significance was set at 0.05. The categorical variables were described as frequency distributions or percentages, and the continuous variables were described as means standard deviations (SD). The association between gender, educational level (primary school or higher than primary school), income (< 20 000 or ≥20 000 Baht), smoking status (none or former/current smoker), plaque index, Thai
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HAQ score, HAQ hand score, salivary flow rate (< 0.70 or >0.70 mL/min), DAS 28 ESR, mean joint erosion score, mean joint space narrowing score, mean total joint erosion and joint space narrowing score and periodontal disease severity, were evaluated using the chi-square or Fisher’s Exact test for discrete variables and the t-test or Mann–Whitney U-test for continuous variables. In order to compare periodontal status of this group of RA patients with the 6th Thailand National Oral Health Survey in the year 2007, we also classified periodontal status according to CPI index and calculated for age–sex adjustment of the Thai population.
RESULTS Two hundred and two patients agreed to participate in the study. Six patients were excluded because of incomplete data; therefore, only 196 patients who had complete data were included in this study. The sociodemograhpic characteristics of the patients are shown in Table 1. Eighty-seven percent of the patients were female. Ninety percent of the patients had incomes that were lower than the Thai average income per household per month (20 903 Baht). Sixty-two percent had a primary school education level. Seventyeight percent had never smoked. Among common co-morbidities, there was hypertension in 62 (30.69%) cases, dyslipidemia in 69 (34.16%), diabetes mellitus in six (2.97%) and chronic kidney disease in five (2.47%). Of 39 patients who had bone density measurements, 23 (58.97%) had osteoporosis and nine (23.08%) had osteopenia. Periodontal findings are shown in Table 1. Mean clinical attachment level was 3.35 0.91 mm. The level of gingival inflammation in this population was low (mean GI index = 0.82 0.46) and oral hygiene was fair (mean PI = 1.21 0.53). Sixty-four percent of the patients had periodontal treatment in the past and 42% had been instructed in the performance of self-care oral hygiene. None had periodontal treatment during the study period. The duration range of RA was 1–32 years (mean 9.62 7.00). Rheumatoid factor (RF) was positive in 82.1% of cases. The range of DAS28 scores was 1.70– 8.56, in which their disease activity was classified as remission, mild, moderate and severe or very active, according to DAS28 criteria of 4.1%, 9.2%, 51.0% and 35.7%, respectively. Despite a majority of the patients having moderate to severe active RA, more than 90% of them had a relatively low Thai HAQ score (mean 0.79 0.68). As only the upper extremity is used for
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Table 1 Socio-demographic, periodontal and medical characteristics of study patients with RA Variables Female n (%) Age (mean SD) Household income/month < 20 000 Baht n (%) Educational level Primary school n (%) Secondary school n (%) University n (%) Smoking status Non-smokers n (%) Periodontal status Remaining teeth (mean SD) Probing depth (mm, mean SD) Clinical attachment level (mm, mean SD) Plaque Index (mean SD) Previous periodontal treatment n (%) Previous oral hygiene instructions n (%) RA status Duration (years, mean SD) RF+ n (%) ESR (mm/h, mean SD) DAS28 (mean SD) Thai HAQ score (mean SD) Upper extremity HAQ score (mean SD) Mean joint erosion score† (mean SD) Mean joint space narrowing score† (mean SD) Total joint erosion and joint space narrowing† (mean SD) Xerostomia n (%) Medications Methotrexate n (%) Prednisolone n (%) Diclofenac n (%) Mono-DMARDs n (%) Combined DMARDs n (%)
171 (87.2) 51.70 9.70 179 (91.3) 122 (62.2) 45 (23) 29 (14.8) 153 (78.1) 25.84 2.28 2.74 0.53 3.35 0.91 1.21 0.53 115 (63.8) 82 (41.8)
9.62 7.00 161 (82.1) 45.76 25.69 4.64 1.25 0.79 0.68 0.66 0.68 36.36 10.41
DISCUSSION
39.92 24.90
In this study, we found a high mean clinical attachment level in this group of Thai patients with RA. According to the CDC-AAP case definitions,36 the periodontal status of this group of patients was classified as moderate and severe periodontits. Only one patient had no periodontitis. This finding was in line with those of previous studies in other countries where a high prevalence of periodontitis in patients with RA was identified (51–70%).8,20,21 However, the prevalence and severity of periodontitis in this study was higher than in others.20,21,37 The reason for such a very high prevalence and severity of periodontal disease in our patients was not clear, but it might be related to the fact that this patient group had a greater severity of RA than patients in other studies appeared to have (86.7% had moderate
76.28 52.69 24 (12.2) 163 (83.2) 111 (56.6) 80 (40.8) 104 (53.1) 78 (39.8)
†Number count from hand radiograph only; RA, rheumatoid arthritis; RF, rheumatoid factor; ESR, erythrocyte sedimentation rate; DAS28, Disease Activity Score of 28 joints; HAQ, Health Assessment Quenstionnaire; DMARDs, disease-modifying antirheumatic drugs.
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dental hygiene care, we therefore calculated only the HAQ score of the upper extremity for analysis. The mean upper extremity HAQ hand score was 0.66 0.68, and 9.7% had upper extremity HAQ >2. The mean salivary flow was 1.44 0.67 mL/min and 12% of patients with RA were classified as having xerostomia. According to the Sharp/van de Heijde score, the patients with RA had a mean joint erosion score, mean joint space narrowing score and mean total joint erosion and joint space narrowing score of 36.36 10.41, 39.92 24.90 and 76.28 52.69, respectively. All patients with RA were treated with one or more medications; 83.2% used methotrexate, 56.6% used prednisolone and 53.1% used mono-disease-modifying antirheumatic drugs. The periodontal status of this population was classified as moderate to severe periodontitis, according to the CDC-AAP case definitions. Only one patient had no periodontitis. The association between sociodemographic characteristics, RA disease characteristics and periodontal parameters between patients who had moderate periodontitis and severe periodontitis is shown in Table 2. Age, male gender, smoking history, number of remaining teeth, plaque index and CAL were significantly different between the two groups of patients. There was no difference in RA variables between patients who had moderate and severe periodontitis. When we used CPI index, 42.6% of the population in the age group 35–44 years had CPI = 3 and 30.1% had CPI = 4. In the age group 60–74 years, 30.8% had CPI = 3 and 69.2% had CPI = 4 (Table 3).
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Table 2 Characteristics of RA and periodontal parameters according to periodontal status
Variables
Male* Age (years)* Household Income < 20 000 Baht/ month Primary school Former/current smokers* Remaining teeth* Plaque index** Mean CAL** Duration of RA (years) DAS28 >3.2 Thai HAQ score >2 Upper extremity; HAQ score >2 Mean joint erosion score Mean joint space narrowing score Mean joint erosion and joint space narrowing score Xerostomia
Moderate periodontitis (n = 83)
Severe periodontitis (n = 112)
5 (6%) 49.48 10.23 75 (90.4%)
19 (17%) 53.37 9.02 103 (92%)
46 (55.4%) 8 (9.6%) 26.34 1.02 2.76 10.00
1.82 0.47 0.45 7.25
75 (67.0%) 34 (30.4%) 25.50 1.37 3.79 9.31
2.51 0.53 0.92 6.85
Pvalue† 0.021 0.006 0.695
0.101 0.001 0.044 < 0.001 < 0.001 0.500
69 (83.1%) 7 (8.4%) 6 (7.2%)
100 (89.3%) 12 (10.7%) 9 (8.0%)
0.211 0.595 0.834
32.80 27.90
39.00 32.15
0.161
37.17 23.41
42.09 25.93
0.174
69.96 48.44
81.09 55.59
0.146
8 (9.6%)
16 (13.9%)
0.329
*P < 0.05, **P < 0.001, †P-values are based on the t-test or Mann–Whitney U-test for continuous data or v2 test for frequency data.
Table 3 Periodontal status of the Thai population in the 6th Thailand National Oral Health Survey (2007) compared to the periodontal status of patients with RA according to CPI index Age group
35–44 60–74
CPI = 3
CPI = 4
Thailand national survey (%)
RA (%)
Thailand national survey (%)
RA (%)
22.1 15.4
42.6 30.8
15.5 68.8
50.1 69.2
to severe active RA and the duration, 9.62 7.00 years, was longer).20,21,37 Although previous reports could not find an association between RA disease severity and periodontitis severity,19,20 the most recent study by Smit et al.37 in 2012 showed a significant finding of severe periodontitis in patients with higher DAS28 scores than in those with no or moderate periodontitis. K€asser et al.38 showed that patients with long-standing, active RA had increased CAL by 173%.
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An important factor that might influence prevalence of periodontitis was the criteria used to classify periodontal disease. There are many periodontal case definitions used in periodontal research.39 The different case definitions have a high impact on prevalence of periodontitis and produce different associations in risk factors of periodontitis.40,41 Some studies used dental radiographs8 or in combination with bleeding on probing and tooth mobility.20 A study in Taiwan, in which a history of periodontal treatment and cumulative costs of the periodontitis-related visit were used to classify peridontitis cases, found a prevalence of periodontitis of 40%.22 However, the use of history and cumulative costs of periodontal treatment raises the issue of accuracy of the diagnostic criteria used to classify periodontitis in their paper. In this study, we classified prevalence and severity of periodontal disease according to CDC-AAP case definitions,36 which was the same criteria used in a study of Indonesian populations.21 These criteria used CAL and PD to determine periodontitis cases. The advantage of using CAL was to measure
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cumulative periodontal destruction in the past, while using only PD may reflect the damage of supporting structure.42 Moreover, we examined all teeth present in the mouth which could reduce a chance of underestimating periodontitis cases compared to partial mouth records in both prevalence and severity of this disease.43 Taken together, the high prevalence of periodontitis cases in our study may reflect the real situation of periodontal disease in our study group. The previous report from the 6th Thailand National Oral Health Survey in the year 2007 found a high prevalence of periodontitis in the Thai general population.44 However, in that study, periodontitis was classified using the Community Periodontal Index (CPI) score, but only PD was reported, which may underestimate prevalence of periodontitis in a high-age population group.45 However, when we modified our data according to the CPI index, we still found that our patients with RA had higher percentages of periodontitis than did the patients in the 6th Thailand National Oral Health Survey (Table 3). These data indicate that the prevalence of periodontitis in Thai patients with RA is high. When we compared RA clinical parameters and periodontal parameters between groups of patients with moderate and severe peridontitis, the result showed that only plaque level, mean CAL, age, male gender and smoking status showed a statistically significant difference. Oral hygiene was a strong risk indicator for periodontitis in the general population.46 However, a study by Pischon et al.19 found that oral hygiene may only partially account for the development of periodontitis in patients with RA. In this study, the average oral hygine level of the patients was fair, and it was in concordance with the upper extremity of the HAQ score, as only 9.7% of the patients had upper extremity HAQ scores >2. Therefore, the ability of the patients in this study group to perform oral hygiene practices might not be impaired by their RA disease severity. Thus, oral hygiene might not play an important role in developing periodontitis in this patient group. Age and male gender have been found as risk indicators for periodontitis.47 Therefore, it was no surprise that those who had severe periodontitis had a higher average age than those with moderate peridontitis. Smoking is also a powerful risk factor for periodontitis47 and it has been shown to be a risk factor for RA development and severity.48 Our results showed a strong association between former/ current smokers and the severe form of peridontitis. This association agreed with other studies, which found higher prevalence and severity of periodontitis in smokers, in a dose-dependent manner.47 Nevertheless,
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it should be noted that most patients in this study were non-smokers. Taken all together, age, oral hygiene and smoking were the only contributing factors for developing the severe form of peridontitis in this population. The factors that might contribute to developing periodontitis in this study group needs to be further elucidated. Our study is the first report of periodontal status in a group of patients with RA in Thailand. The information from our study might merit further investigation for advanced knowledge regarding the relationship between RA disease and periodontitis. Our study population was quite large, compared to some other previous reports.19,37 To minimize under- or over-estimation, we included only subjects who had 20 teeth or more (excluding third molars) and all presenting teeth were examined. Therefore, the periodontal conditions in our patients with RA represented the true status of the study population. Some of the previous studies had reported the numbers of teeth lost, but the reasons for the loss were not mentioned.18,19 In fact, the major causes of tooth loss in the general population are dental caries and periodontal disease.49 The only important reason for tooth loss in these studies was from periodontal disease, which might influence the interpretation of the results. Our study had some limitations. It was a cross-sectional study and did not have a control group; so we could not compare potential risk factors for having periodontitis in this study population. Another limitation was the lack of intra-oral radiographs in this study, resulting in an inability to measure the level of bone loss and compare it with periodontal clinical parameters. However, in this study, we measured the clinical attachment level, which has been shown to have a relationship with bone loss.50 Thus, the periodontal status in our study may represent the level of periodontal destruction in a Thai population with RA. Lastly, we did not have a chance to measure anti-citrullinated peptide antibodies (ACPA) in our RA patients, as by the time of the study, the ACPA test was very expensive and was not routinely available at our hospital. Future study of the association of ACPA and periodontitis might be of interest.
CONCLUSIONS In this study, we found that Thai patients with RA had a high prevalence of moderate or severe periodontal disease. Increasing age, male gender, previous or current smoking and a high plaque score were associated with severity of periodontal disease. The RA clinical
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parameters, the medication used and the upper extremity HAQ score showed no association with moderate or severe periodontal disease in this population.
ACKNOWLEDGEMENTS The authors thank Mrs. Woraporn Sukittawut, B.Sc. and Rheumatology staff for their secretarial assistance. This study was supported by a graduate thesis grant, Faculty of Dentistry, Chiang Mai University. The authors also thank Dr. M. Kevin O’Carroll, Professor Emeritus of the University of Mississippi School of Dentistry, USA and Faculty Consultant at Chiang Mai University Faculty of Dentistry, Thailand, for his critical reading of this manuscript.
CONFLICT OF INTEREST All authors declare no conflict of interest.
REFERENCES 1 Page RC, Offenbacher S, Schroeder HE, Seymour GJ, Kornman KS (1997) Advances in the pathogenesis of periodontitis: summary of developments, clinical implications and future directions. Periodontol 2000 14, 216–48. 2 Mealey BL, Oates TW (2006) Diabetes mellitus and periodontal diseases. J Periodontol 77, 1289–303. 3 Offenbacher S, Katz V, Fertik G et al. (1996) Periodontal infection as a possible risk factor for preterm low birth weight. J Periodontol 67, 1103–13. 4 Beck J, Garcia R, Heiss G, Vokonas PS, Offenbacher S (1996) Periodontal disease and cardiovascular disease. J Periodontol 67, 1123–37. 5 Rutger Persson G, Ohlsson O, Pettersson T, Renvert S (2003) Chronic periodontitis, a significant relationship with acute myocardial infarction. Eur Heart J 24, 2108–15. 6 Grau AJ, Becher H, Ziegler CM et al. (2004) Periodontal disease as a risk factor for ischemic stroke. Stroke 35, 496– 501. 7 Al-Shammari KF, Al-Khabbaz AK, Al-Ansari JM, Neiva R, Wang HL (2005) Risk indicators for tooth loss due to periodontal disease. J Periodontol 76, 1910–8. 8 Mercado F, Marshall RI, Klestov AC, Bartold PM (2000) Is there a relationship between rheumatoid arthritis and periodontal disease? J Clin Periodontol 27, 267–72. 9 Persson LO, Berglund K, Sahlberg D (1999) Psychological factors in chronic rheumatic diseases–a review. The case of rheumatoid arthritis, current research and some problems. Scand J Rheumatol 28, 137–44. 10 Antoniazzi RP, Miranda LA, Zanatta FB et al. (2009) Periodontal conditions of individuals with Sjogren’s syndrome. J Periodontol 80, 429–35.
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11 Berthelot JM, Le Goff B (2010) Rheumatoid arthritis and periodontal disease. Joint Bone Spine 77, 537–41. 12 Rosenstein ED, Greenwald RA, Kushner LJ, Weissmann G (2004) Hypothesis: the humoral immune response to oral bacteria provides a stimulus for the development of rheumatoid arthritis. Inflammation 28, 311–8. 13 Bartold PM, Marino V, Cantley M, Haynes DR (2010) Effect of Porphyromonas gingivalis-induced inflammation on the development of rheumatoid arthritis. J Clin Periodontol 37, 405–11. 14 Martinez-Martinez RE, Abud-Mendoza C, Patino-Marin N, Rizo-Rodriguez JC, Little JW, Loyola-Rodriguez JP (2009) Detection of periodontal bacterial DNA in serum and synovial fluid in refractory rheumatoid arthritis patients. J Clin Periodontol 36, 1004–10. 15 Nesse W, Westra J, van der Wal JE et al. (2012) The periodontium of periodontitis patients contains citrullinated proteins which may play a role in ACPA (anti-citrullinated protein antibody) formation. J Clin Periodontol 39, 599–607. 16 Bonfil JJ, Dillier FL, Mercier P et al. (1999) A “case control” study on the role of HLA DR4 in severe periodontitis and rapidly progressive periodontitis. Identification of types and subtypes using molecular biology (PCR.SSO). J Clin Periodontol 26, 77–84. 17 Ishida K, Kobayashi T, Ito S et al. (2012) Interleukin-6 gene promoter methylation in rheumatoid arthritis and chronic periodontitis. J Periodontol 83, 917–25. 18 Mercado FB, Marshall RI, Klestov AC, Bartold PM (2001) Relationship between rheumatoid arthritis and periodontitis. J Periodontol 72, 779–87. 19 Pischon N, Pischon T, Kroger J et al. (2008) Association among rheumatoid arthritis, oral hygiene, and periodontitis. J Periodontol 79, 979–86. 20 Dissick A, Redman RS, Jones M et al. (2010) Association of periodontitis with rheumatoid arthritis: a pilot study. J Periodontol 81, 223–30. 21 Susanto H, Nesse W, Kertia N et al. (2013) Prevalence and severity of periodontitis in indonesian patients with rheumatoid arthritis. J Periodontol 84, 1067–74. 22 Chen HH, Huang N, Chen YM et al. (2013) Association between a history of periodontitis and the risk of rheumatoid arthritis: a nationwide, population-based, case-control study. Ann Rheum Dis 72, 1206–11. 23 Sjostrom L, Laurell L, Hugoson A, Hakansson JP (1989) Periodontal conditions in adults with rheumatoid arthritis. Community Dent Oral Epidemiol 17, 234–6. 24 Kobayashi T, Murasawa A, Komatsu Y et al. (2010) Serum cytokine and periodontal profiles in relation to disease activity of rheumatoid arthritis in Japanese adults. J Periodontol 81, 650–7. 25 de Pablo P, Dietrich T, McAlindon TE (2008) Association of periodontal disease and tooth loss with rheumatoid arthritis in the US population. J Rheumatol 35, 70–6. 26 Havemose-Poulsen A, Westergaard J, Stoltze K et al. (2006) Periodontal and hematological characteristics
517
N. Khantisopon et al.
27
28
29
30
31
32
33
34
35 36
37
38
associated with aggressive periodontitis, juvenile idiopathic arthritis, and rheumatoid arthritis. J Periodontol 77, 280–8. Arnett FC, Edworthy SM, Bloch DA et al. (1988) The American Rheumatism Association 1987 revised criteria for the classification of rheumatoid arthritis. Arthritis Rheum 31, 315–24. Smolen JS, Breedveld FC, Eberl G et al. (1995) Validity and reliability of the twenty-eight-joint count for the assessment of rheumatoid arthritis activity. Arthritis Rheum 38, 38–43. Osiri M, Deesomchok U, Tugwell P (2001) Evaluation of functional ability of Thai patients with rheumatoid arthritis by the use of a Thai version of the Health Assessment Questionnaire. Rheumatology (Oxford) 40, 555–8. van der Heijde D (2000) How to read radiographs according to the Sharp/van der Heijde method. J Rheumatol 27, 261–3. Jensen JL, Karatsaidis A, Brodin P (1998) Salivary secretion: stimulatory effects of chewing-gum versus paraffin tablets. Eur J Oral Sci 106, 892–6. Malmstrom MJ, Segerberg-Konttinen M, Tuominen TS et al. (1988) Xerostomia due to Sjogren’s syndrome. Diagnostic criteria, treatment and outlines for a continuous dental care programme and an open trial with Sulfarlem. Scand J Rheumatol 17, 77–86. The Household Socio-Economic Survey (2009) (Internet). National Statistical Office, Bangkok. [Cited 6 Apr 2013.] Available from: http://www.nso.go.th. Silness J, Loe H (1964) Periodontal disease in pregnancy. Ii. Correlation between oral hygiene and periodontal condition. Acta Odontol Scand 22, 121–35. Loe H, Silness J (1963) Periodontal disease in pregnancy I. Prevalence and severity. Acta Odontol Scand 21, 533–51. Eke PI, Page RC, Wei L, Thornton-Evans G, Genco RJ (2012) Update of the case definitions for population-based surveillance of periodontitis. J Periodontol 83, 1449–54. Smit MD, Westra J, Vissink A, Doornbos-van der Meer B, Brouwer E, van Winkelhoff AJ (2012) Periodontitis in established rheumatoid arthritis patients: a cross-sectional clinical, microbiological and serological study. Arthritis Res Ther 14, R222. K€asser UR, Gleissner C, Dehne F, Michel A, WillershausenZonnchen B, Bolten WW (1997) Risk for periodontal disease in patients with longstanding rheumatoid arthritis. Arthritis Rheum 40, 2248–51.
518
39 Savage A, Eaton KA, Moles DR, Needleman I (2009) A systematic review of definitions of periodontitis and methods that have been used to identify this disease. J Clin Periodontol 36, 458–67. 40 Costa FO, Guimaraes AN, Cota LO et al. (2009) Impact of different periodontitis case definitions on periodontal research. J Oral Sci 51, 199–206. 41 Kassab P, Colombier ML, Kaminski M, Lelong N, Sixou M, Nabet C (2011) Impact of periodontitis definition in epidemiological research. Results from the EPIPAP study in postpartum women. Eur J Oral Sci 119, 156–62. 42 Beltran-Aguilar ED, Eke PI, Thornton-Evans G, Petersen PE (2012) Recording and surveillance systems for periodontal diseases. Periodontol 2000 60, 40–53. 43 Kingman A, Susin C, Albandar JM (2008) Effect of partial recording protocols on severity estimates of periodontal disease. J Clin Periodontol 35, 659–67. 44 The 6th Thailand National Oral Health Survey (2007) (Internet). Department of Health, Ministry of Health, Bangkok. [Cited 10 Feb 2014.] Available from: http:// dental.anamai.moph.go.th/oral health/PR/E-book/Survey/ survey6th.pdf. 45 Baelum V, Manji F, Wanzala P, Fejerskov O (1995) Relationship between CPITN and periodontal attachment loss findings in an adult population. J Clin Periodontol 22, 146– 52. 46 Tanner AC, Kent R Jr, Van Dyke T, Sonis ST, Murray LA (2005) Clinical and other risk indicators for early periodontitis in adults. J Periodontol 76, 573–81. 47 Torrungruang K, Nisapakultorn K, Sutdhibhisal S et al. (2005) The effect of cigarette smoking on the severity of periodontal disease among older Thai adults. J Periodontol 76, 566–72. 48 Navarro-Compan V, Melguizo-Madrid E, Hernandez-Cruz B et al. (2013) Interaction between oxidative stress and smoking is associated with an increased risk of rheumatoid arthritis: a case-control study. Rheumatology (Oxford) 52, 487–93. 49 Beltran-Aguilar ED, Beltran-Neira RJ (2004) Oral diseases and conditions throughout the lifespan. I. Diseases and conditions directly associated with tooth loss. Gen Dent 52, 21–7. 50 Goodson JM, Haffajee AD, Socransky SS (1984) The relationship between attachment level loss and alveolar bone loss. J Clin Periodontol 11, 348–59.
International Journal of Rheumatic Diseases 2014; 17: 511–518
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