Orthopedics
Stomatognathic system involvement in rheumatoid arthritis patients Andrea E. Bono1, Jorge Alfonso Learreta2, Graciela Rodriguez3, Juan Carlos Marcos3,4 1
National University of La Plata (UNLP), Argentina, 2TMJ Department, Argentine Society for Orthodontics, Buenos Aires, Argentina, 3Rheumatology Service, H.I.G.A., La Plata, Argentina, 4Department of Rheumatology, National University of La Plata (UNLP), Argentina Aims: Temporomandibular joint (TMJ) and stomatognathic system involvement are usually observed during the course of rheumatoid arthritis. Methodology: This article presents the findings during examination of 190 TMJs from rheumatoid arthritis (RA) patients, and 44 TMJs from controls without RA, including a description of signs and symptoms related to the stomatognathic system, radiological findings in hands-, and TMJ, erythrocyte sedimentation rate (ESR) values, and scores obtained in the Disease Activity Score (Das 28) and the Health Assessment Questionnaire (HAQ). Results: The sample included 57.89% TMJs associated with spontaneous pain, 87.89% with signs of destruction in radiological images, and 58.94% with 20 teeth or less. Restricted mouth opening was detected in 42.1% of RA patients, from which 71% had blocked opening; headache was present in 58%, and pain in the masticatory muscles was found in 57%. TMJ erosions had a significant association with Larsen scores (r50.62), but not with the Das 28, HAQ, and ESR values. Conclusions: The early evaluation of this joint and the collaborative work of odontologists and rheumatologists are both necessary for a better management of TMJ pathologies.
Keywords: Temporomandibular joint, Rheumatoid arthritis, DAS 28, HAQ
Introduction Rheumatoid arthritis (RA) is an autoimmune inflammatory disease that involves the diarthrodial joints of the body, including the temporomandibular joint (TMJ). In the latter case, articular involvement produces pain, impaired mouth opening, and crepitations.1–5 According to recent studies, the prevalence of AR in Argentina is 1%.6 In the most severe cases of TMJ involvement, the masticatory movements and the stomatognathic system may be affected. The prevalence of TMJ disorders in RA patients varies widely, so that rates from 4.7% to 88% have been reported. Bracco et al.7 reported TMJ involvement in 53–93% of the patients, while Lin et al.8 reported radiological TMJ abnormalities in 74.5%, and functional abnormalities in 85.7%. Ogus9 found affected TMJ in 61% of the symptomatic patients. Studies on histocompatibility antigens performed by Helenius et al.10 showed a significant association between HLADRB1-01 and
Correspondence to: JA Learreta, Univ Catolica de Salta, Beruti 3208 2-Piso, Buenos Aires 1425, Argentina. Email: [email protected] ß W. S. Maney & Son Ltd 2014 DOI 10.1179/0886963413Z.0000000003
destructive lesions of the TMJ, while Learreta et al.11 found a significant association with DR1, DR4, and DR7 antigens. According to these authors, the predominant local symptoms were pain and opening difficulties due to the reduced translation movement of the condyle. Akerman et al.12 found that the severity of radiological abnormalities in the TMJ were comparable to those found in the metacarpophalangeal joints of hands and feet, assessed by the Larsen method.13 Usually, the TMJ is not assessed by rheumatologists, who center their attention in other joints. Nevertheless, the TMJ may be severely affected, presenting sequelae and dysfunction. Therefore, the goal of the present study was to assess in RA patients the clinical signs and symptoms of TMJ from an odontological and rheumatological point of view, analyzing potential relationships between the different measures. The authors’ hypothesis was that the identification of the most important predictors of the disease would facilitate the diagnosis and early treatment of TMJ disorders in RA patients.
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Materials and Methods Patients The study included 100 consecutive patients (83 females and 17 males) assisted in the Rheumatology Service of the San Martı´n Hospital in La Plata, Argentina, who met the RA criteria of the American College of Rheumatology. The study was approved by the Ethics Committee of the San Martı´n Hospital. The control group included 22 healthy volunteers who met the inclusion criteria and none of the exclusion criteria. For the RA group, inclusion criteria included having RA according to the American College of Rheumatology,14 being over 18 years old, and signing the informed consent form approved by the Ethics Committee, which was prepared in accordance to the Helsinki Declaration and good medical practices. Exclusion criteria for the RA group were concomitant immunological diseases, fibromyalgia, lupus, ankylosing spondylitis, or juvenile RA at the time of clinical or radiological examination, or having previous TMJ surgery. From the 100 patients initially recruited, 95 met the inclusion criteria and completed the study. The remainder were excluded because of deficient radiological films or incomplete serological data. The mean age of RA patients was 45 years (range: 24–74 years), and the mean duration of the disease was 10.5 years (range: 2–39 years). The mean age of the control group was 42 years (range: 35–52 years). Patients were examined by both a rheumatologist and an odontologist. The study included 190 TMJs considered in unilateral form.
Clinical examination All patients were evaluated using a detailed questionnaire of the stomatognathic system. The odontological evaluation of this system included: (a) painful points related to the TMJ: (a.1) external auditory discitis (retrodiscitis); (a.2) TMJ pain closing or opening the mouth (malposition of the condyle or disc); (b) tinnitus or otodynia; (c) maximal mouth opening (considering a normal range between 40 and 45 mm); (d) lower facial height, (e) crepitations; (f) clicks; (g) masticatory muscles; and (h) headaches. The rheumatological evaluation included the determination of acute phase reactants (erythrocyte sedimentation rate, ESR), disease activity (Disease Activity Score, Das 28), and functional capacity (Health Assessment Questionnaire, HAQ). Das 2815 is the best index to evaluate and discriminate between high and low disease activity in RA patients, since it takes into consideration painful joints, swollen joints, ESR, and a global disease rating. Its results are translated into disease activity levels as follows: (3.2 low activity, .3.2 and (5.1 moderate 32
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activity, and .5.1 high activity. The HAQ16 questionnaire evaluates functional impairment and work disability, and consists of 20 questions including difficulty for dressing, personal hygiene, eating, walking, and holding, among others. For each category, assigned values vary between 0 (no difficulty) and 3 (unable to perform the task). A HAQ value .1.25 reflects severe disease.
Radiological examination TMJ Green-sensitive X-ray films measuring 24630 cm (AGFAH) were used in the current study. Two images were taken for each TMJ with linear tomograph technique, one with open mouth and the other in maximal occlusion. Evaluation was performed using the Rohlin–Petersson method,13,17 modified by Larsen, which rates TMJ according to erosion severity as follows (Fig. 1): grade 15normal conditions: welldefined condylar and glenoid shape, with convex cortical; grade 25slightly abnormal: minor changes such as osteophytes, crushing, and sclerosis. Uncertain findings are also included in this grade; grade 35moderate destructive abnormality: local erosions and changes; grade 45severe destructive abnormality: extensive erosions in the condyle and the temporal bone, with medial and lateral extension; and grade 55mutilating abnormalities: total erosion of the condyle with loss of articular surfaces and ankylosis. Hands The carpal technique was used with a focus/film distance of 1 m, without angulation, with the focal point in the metacarpo-phalangeal joint. Comparative films from both hands were requested. The radiological evaluation was performed with the Larsen method,13 which includes the assessment of the 2nd, 3rd, 4th and 5th metacarpo-phalangeal joints, second, third, fourth, and fifth proximal interphalangeal joints, and the carpus, considered in four sections: two upper sections and two lower ones. A value was adjudicated to each joint according to the abnormalities observed, which were summed to obtain the total value for each hand. Larsen grades were as follows: grade 05intact articular shape and preserved interarticular space; grade 15mild erosions lower than 1 mm, and slight reduction of the articular space, juxtaarticular osteoporosis, or soft tissue swelling; grade 25articular space reduced by less than 50%, with preserved joint and erosion greater than 1 mm; grade 35articular space reduced by more than 50% and marked erosion; grade 45osteal ankylosis with partially preserved bone shape; grade 55osteal ankylosis without preserved bone shape. VOL .
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Figure 1 Normal TMJ and hand, and assessment of right hand and right TMJ in a RA patient having the disease for a duration of 15 years. A reduction of the articular space in the carpus, with collapses and ankylosis, can be observed in the hand, together with reduced osteal shape in the second, third, fourth, and fifth metacarpophalangeal joints. A reduced osteal shape with ankylosis can also be observed in the second, third, fourth, and fifth proximal joints. The TMJ presents a grade 3 severity on the Rohlin–Petersson scale, including moderately destructive abnormality, erosive changes of the anterior and posterior condylar surface, and reduction of the articular space.
Statistical analysis
Frequency and presentation of TMJ pathologies
The statistical measures of position and dispersion were calculated for each variable. A retrospective case–control observational design was implemented to evaluate the prevalence of TMJ pathologies in 100 patients with RA. For statistical analysis, the authors calculated statistical measures of dispersion and position for each variable. The test used to compare differences in percentages is the test of differences in proportions (P). To study the strength of associations between two variables, the authors used the Pearson correlation coefficient (R).
The RA sample included 95 patients (84% female and 16% male) with a mean age of 45 years and a mean disease duration of 10.5 years (range: 2–39 years). Based on the questionnaire, headache was present in 53 (58%) of the RA patients, masticatory muscle pain was present in 57%, shoulder pain was present in 56%, and forefront pain was present in 33%. The clinical examination disclosed impaired mouth opening in 40 cases (42.1%) and reduced mouth opening (less than 40 mm) in 67 (71%), which was significantly more frequent than in the control group (13.6% with reduced opening).
Results RA severity
Table 1 Sample distribution
The severity of RA in the 95 patients, and the results of the clinical, radiological, and laboratory evaluations are shown in Tables 1 and 2.
Variable Sex (female/male) Age, mean (range) RA duration, mean (range)
84%/16% 45 years (24–74 years) 10.5 years (2–39 years)
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Table 2 Comparison between groups using the proportion differences test (P)* Frequency and presentation of stomatognathic system findings Clinical findings
Questionnaire
Impaired mouth opening Impaired mastication Dental pieces lost (less than 20 remaining) Reduced maximal opening Blocked opening from reduced maximal opening group ERS (mm/h) Headache TMJ pain TMJ clicks TMJ crepitations Masticatory muscles pain Shoulders pain Forefront pain
RA (n595)
Control (n522)
P
32 23 56 40 67
3 (14%) 3 (14%) 0% 3 (13.6%) 0%
0.073 0.508 … 0.000 0.000
2 (9.1%) 8 (36.36)% Control (n544) 1 (2.27%) 1 (2.27%) 8 (18.18%) 2% 0 0
0.004 H/S 0.339(N/S) P* 0.000 (H/S) 0.000 (H/S) 0,0065 (N/S) 0.000 (H/S)
(33.68%) (23.24%) (58.94%) (42.1%) (71%)
43 (45.3%) 53 (58%) AR (n5190) 57.89% (109) 110 (55.78%) 80 (42.10%) 57% 56% 33%
(N/S) (N/S) (H/S) (H/S)
Note: *P: proportion differences test. RA, rheumatoid arthritis; TMJ, temporomandibular joint; H/S, highly significant association; S, significant association; N/S, nonsignificant association.
Other abnormalities detected were clicks, which were significantly more frequent in RA joints than in those of the control group (55.78% versus 2.27%, P50.000), and crepitations, which were detected in 80 TMJs (42.10%, not significantly different from the control group; P50.065). Pain was present in 109 TMJs from RA patients (57.89%), being unilateral in 82 cases (75.24%) and bilateral in 27 (24.77%). The Das 28 index revealed a high disease activity in 31.34% of RA patients, moderate activity in 47.51%, and low activity in 14.15%. In contrast, it indicated low disease activity in all the individuals from the control group. The HAQ yielded values between 0 and 0.5 in 43% of the cases, and between 0.5 and 1 in 21%, thus showing that RA patients did not exhibit an important functional impairment. In the control group, the HAQ value was 0 in 95% of the cases, and only one individual presented a value of 1.1. ESR values (upper reference value 30 mm) were increased in 40.85% of RA patients, while 59% of controls had values between 11 and 20 mm. Radiological studies revealed that 168 (88.42%) of the 190 TMJs evaluated had some degree of erosion, according to the Rholin–Petersson classification, together with condylar destruction, deformity or integrity loss (Table 3). Twelve joints per hand were evaluated, so in 95 patients, 1140 joints per side, or a total of 2280 joints were evaluated. Some degree of erosion was detected in almost 80% of these joints.
Table 3 Classification of TMJ erosion degree according to the Rholin–Petersson score TMJ erosion stages according to Rholin–Petersson TMJ classification (n5190)
Control (n544)
P
Grade 0 Grade 1 Grade 2 Grade 3 Grade 4 Grade 5 Unclassified
42 (95.45%) 2 (4.54%) 0 0 0 0 0
0.000 H/S 0.005 H/S … … … … …
22 (11.57%) 34 (17.89%) 49 (25.78%) 45 (23.68%) 31 (16.31%) 8 (4.21%) 1(0.52%)
Note: *P: proportion differences test. H/S, highly significant association; N/S, non-significant association.
in the hands, according to Larsen classification. In contrast, TMJ erosions were not significantly associated with Das 28 scores (r50.28), HAQ values (r50.07), or ESR values (r50.07) (Fig. 2 and Table 5).
Association analysis A highly significant association (r50.62) was found between TMJ erosions and radiological findings 34
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Figure 2 Association between Larsen scores and Rholin– Petersson scores (Pearson correlation coefficient r).
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Table 4 Classification of hand erosion degree according to the score of Larsen Erosion degree in hands according to Larsen
Affected hand joints in RA patients (n)
Affected hand joints in RA patients (%)
Affected hand joints in control group (n)
Affected hand joints in control group (%)
P*
Grade 0 Grade 1 Grade 2 Grade 3 Grade 4 Grade 5 Unclassified
457 588 462 366 190 193 24
20.04 25.78 20.26 16.05 8.33 9.46 1.05
503 25 0 0 0 0 0
95.26 4.73 0 0 0 0 0
P50.000 H/S P50.002 H/S … … … … …
Note: *P: proportion differences test. H/S, highly significant association.
Table 5 Association between the Rholin–Petersson scores and the Larsen scores, Das 28, HAQ, and ESR values ATM
Larsen
ERS
HAQ
DAS 28
r Sign.
0.62 AS
0.07 NS
0.07 NS
0.28 NS
To study the strength of associations between two variables, the Pearson’s correlation coefficient r, not P was used.
Discussion The majority of individuals from the two groups included in the present study were females. Among RA patients, the proportion of females was 83%, which is in agreement with previous reports on the gender distribution of RA.18–23 Headache was present in 58% of RA patients, in concordance with the study by Koh et al.,24 who found this complaint in 47.5% of 80 patients with RA evaluated for temporomandibular disorders. TMJ pain was detected in 57.89% of the RA patients included in the present study, which agrees with the findings of Kallemberg and Scuttelari,18,25 who concluded that RA patients are prone to develop TMJ pain at different times, according to RA flares. Previous studies by Wort et al.26 mention infrequent TMJ pain among patients with rheumatic diseases, and attribute these complaints to myalgias, fibrositis, and ligaments pain, which is in contrast to the findings in the current study, in which 57.89% of the RA patients had TMJ pain. Given the presence of bone erosions and the close up of osteal insertions, it is expected that pain in the articular region is due to RA rather than to other conditions of myogenic origin. TMJ clicks were detected in 55.78% of the RA patients at the time of examination. Similarly, EttalaYlitalo et al.27 found TMJ clicks in 53.3% of 60 RA patients, and Ozcan et al.28 found this type of sounds in 48.8% of 43 RA patients. Owing to bone lesions in TMJ and the diminished space for the articular disc, an osteal
friction on a soft tissue of TMJ may exist, producing the clicks detected in patients. The percentages of patients having clicks and crepitations were higher in this study than those reported by Koh et al.,24 who found these sounds in 21.3% and 27.5%, respectively. The presence of crepitations is frequent in inflammatory and degenerative disorders, as revealed by other studies.12,20,29,30 Crepitations were prevalent in the RA patients included in the present study, being unilateral in 26.31% of the cases and bilateral in 15.78%, yielding a total prevalence of 42.10%. According to Hajati and Wiese,31,32 crepitation is a clinical sign of condylar surface destruction in chronic arthritis, and correlates with radiological signs of erosion in TMJ and hands, potentially constituting a predictor of bone erosion. From the RA patients evaluated, 58.94% presented less than 20 teeth (most of them being posterior teeth — first or second molars), which differs markedly from the control group in which 77.27% of the patients had more than 20 teeth. This may be related to the positive association between periodontal disease and RA reported by Mercado et al. and Garib and Qaradaxi.33,34 The maximal mouth opening was diminished in 42.5% of the RA patients included in the current study, in line with the findings of Angyal et al.35 and Yilmaz et al.,36 and the mouth opening was restricted in 67 cases (71%). Some type of erosion was detected in 85.77% of the joints assessed. This is coincident with several previous studies37–39 that included radiological evaluation of TMJ. However, not all the evaluation tests considered the bone surface, the free space available for the disc, and the presence of osteophytes and facets as the Rholin–Petersson method does. In agreement with the report by Tsiklaki,40 the radiological examination had an important role in the diagnosis of TMJ pathologies. No significant association was found between HAQ, DAS, or ESR values and the TMJ findings,
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thus showing that TMJ lesions do not correlate with disease activity, so that TMJ may be affected in varying degrees during the acute stage of RA. This may be due to the fact that Das 28 and HAQ do not consider functions of the stomatognathic system such as eating, speaking, or yawning. As these functions are among the ones that are impaired in RA patients, their inclusion in the HAQ may help detect some incapacity at joint or dental levels. Future studies should modify this questionnaire by including some of these variables, thus contributing to the early detection of TMJ impairments in RA patients. The most relevant radiological findings were erosion of the condylar surface, subcortical sclerosis of the condyle, and diminution of the space for the articular disc. Erosions in the hands were significantly associated with radiological findings in TMJ (r50.62) using the Rholin–Petersson method. To the best of the authors’ knowledge, this study is the first to establish an association between both variables. This allows the rheumatologist to predict that patients with bone erosions in the hands will likely have some type of TMJ lesion, making necessary the referral to an odontologist for treatment of the joint affected by RA.
Conclusions A highly significant association was found in the present study between headache and TMJ erosions. TMJ pain was present in 57.89% of RA patients, clicks were detected in 55.78%, crepitations were found in 42.10%, TMJ pain at rest was reported by 53.51%, and 58.94% of the patients had fewer than 20 teeth, thus lacking dental support. Mouth opening was diminished in 42.1% of the patients and was blocked in 71%. Based on radiological evaluation of TMJ, 25.8%, 23.68%, and 16.31% of the patients were classified into groups 2, 3, and 4 of Rholin–Petersson, respectively. According to carpal Rx films, 25.78%, 20.26%, and 16.05% of the RA patients were classified into grade 1, 2 and 3 of Larsen, respectively, whereas 96.02% of individuals from the control group were classified into group 0. A highly significant association was found between TMJ erosions graded according to the method of Rholin–Petersson and the carpal radiological findings classified according to the method of Larsen. In contrast, no association was found between TMJ erosions and HAQ, DAS, or ESR values. Signs of TMJ pathologies should be systematically sought in RA patients to allow their early detection, since clinical symptoms frequently attributed to muscle contracture can be caused by such pathologies. The authors propose to start such assessment 36
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from the early stages of RA, as this may facilitate the diagnosis and treatment of TMJ disorders. All rheumatologic patients should be screened. The maintenance of an adequate dental support may avoid an aggravating factor for the progressive TMJ damage during RA. The collaborative work between rheumatologists and odontologists may lead to an early diagnosis of TMJ disorders, allowing the design of combined therapeutic strategies aimed at minimizing the damage to an important joint with indispensable functions for human life.
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Stomatognathic system involvement in rheumatoid arthritis patients Andrea E. Bono1, Jorge Alfonso Learreta2, Graciela Rodriguez3, Juan Carlos Marcos3,4 1
National University of La Plata (UNLP), Argentina, 2TMJ Department, Argentine Society for Orthodontics, Buenos Aires, Argentina, 3Rheumatology Service, H.I.G.A., La Plata, Argentina, 4Department of Rheumatology, National University of La Plata (UNLP), Argentina Aims: Temporomandibular joint (TMJ) and stomatognathic system involvement are usually observed during the course of rheumatoid arthritis. Methodology: This article presents the findings during examination of 190 TMJs from rheumatoid arthritis (RA) patients, and 44 TMJs from controls without RA, including a description of signs and symptoms related to the stomatognathic system, radiological findings in hands-, and TMJ, erythrocyte sedimentation rate (ESR) values, and scores obtained in the Disease Activity Score (Das 28) and the Health Assessment Questionnaire (HAQ). Results: The sample included 57.89% TMJs associated with spontaneous pain, 87.89% with signs of destruction in radiological images, and 58.94% with 20 teeth or less. Restricted mouth opening was detected in 42.1% of RA patients, from which 71% had blocked opening; headache was present in 58%, and pain in the masticatory muscles was found in 57%. TMJ erosions had a significant association with Larsen scores (r50.62), but not with the Das 28, HAQ, and ESR values. Conclusions: The early evaluation of this joint and the collaborative work of odontologists and rheumatologists are both necessary for a better management of TMJ pathologies.
Keywords: Temporomandibular joint, Rheumatoid arthritis, DAS 28, HAQ
Introduction Rheumatoid arthritis (RA) is an autoimmune inflammatory disease that involves the diarthrodial joints of the body, including the temporomandibular joint (TMJ). In the latter case, articular involvement produces pain, impaired mouth opening, and crepitations.1–5 According to recent studies, the prevalence of AR in Argentina is 1%.6 In the most severe cases of TMJ involvement, the masticatory movements and the stomatognathic system may be affected. The prevalence of TMJ disorders in RA patients varies widely, so that rates from 4.7% to 88% have been reported. Bracco et al.7 reported TMJ involvement in 53–93% of the patients, while Lin et al.8 reported radiological TMJ abnormalities in 74.5%, and functional abnormalities in 85.7%. Ogus9 found affected TMJ in 61% of the symptomatic patients. Studies on histocompatibility antigens performed by Helenius et al.10 showed a significant association between HLADRB1-01 and
Correspondence to: JA Learreta, Univ Catolica de Salta, Beruti 3208 2-Piso, Buenos Aires 1425, Argentina. Email: [email protected] ß W. S. Maney & Son Ltd 2014 DOI 10.1179/0886963413Z.0000000003
destructive lesions of the TMJ, while Learreta et al.11 found a significant association with DR1, DR4, and DR7 antigens. According to these authors, the predominant local symptoms were pain and opening difficulties due to the reduced translation movement of the condyle. Akerman et al.12 found that the severity of radiological abnormalities in the TMJ were comparable to those found in the metacarpophalangeal joints of hands and feet, assessed by the Larsen method.13 Usually, the TMJ is not assessed by rheumatologists, who center their attention in other joints. Nevertheless, the TMJ may be severely affected, presenting sequelae and dysfunction. Therefore, the goal of the present study was to assess in RA patients the clinical signs and symptoms of TMJ from an odontological and rheumatological point of view, analyzing potential relationships between the different measures. The authors’ hypothesis was that the identification of the most important predictors of the disease would facilitate the diagnosis and early treatment of TMJ disorders in RA patients.
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Materials and Methods Patients The study included 100 consecutive patients (83 females and 17 males) assisted in the Rheumatology Service of the San Martı´n Hospital in La Plata, Argentina, who met the RA criteria of the American College of Rheumatology. The study was approved by the Ethics Committee of the San Martı´n Hospital. The control group included 22 healthy volunteers who met the inclusion criteria and none of the exclusion criteria. For the RA group, inclusion criteria included having RA according to the American College of Rheumatology,14 being over 18 years old, and signing the informed consent form approved by the Ethics Committee, which was prepared in accordance to the Helsinki Declaration and good medical practices. Exclusion criteria for the RA group were concomitant immunological diseases, fibromyalgia, lupus, ankylosing spondylitis, or juvenile RA at the time of clinical or radiological examination, or having previous TMJ surgery. From the 100 patients initially recruited, 95 met the inclusion criteria and completed the study. The remainder were excluded because of deficient radiological films or incomplete serological data. The mean age of RA patients was 45 years (range: 24–74 years), and the mean duration of the disease was 10.5 years (range: 2–39 years). The mean age of the control group was 42 years (range: 35–52 years). Patients were examined by both a rheumatologist and an odontologist. The study included 190 TMJs considered in unilateral form.
Clinical examination All patients were evaluated using a detailed questionnaire of the stomatognathic system. The odontological evaluation of this system included: (a) painful points related to the TMJ: (a.1) external auditory discitis (retrodiscitis); (a.2) TMJ pain closing or opening the mouth (malposition of the condyle or disc); (b) tinnitus or otodynia; (c) maximal mouth opening (considering a normal range between 40 and 45 mm); (d) lower facial height, (e) crepitations; (f) clicks; (g) masticatory muscles; and (h) headaches. The rheumatological evaluation included the determination of acute phase reactants (erythrocyte sedimentation rate, ESR), disease activity (Disease Activity Score, Das 28), and functional capacity (Health Assessment Questionnaire, HAQ). Das 2815 is the best index to evaluate and discriminate between high and low disease activity in RA patients, since it takes into consideration painful joints, swollen joints, ESR, and a global disease rating. Its results are translated into disease activity levels as follows: (3.2 low activity, .3.2 and (5.1 moderate 32
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activity, and .5.1 high activity. The HAQ16 questionnaire evaluates functional impairment and work disability, and consists of 20 questions including difficulty for dressing, personal hygiene, eating, walking, and holding, among others. For each category, assigned values vary between 0 (no difficulty) and 3 (unable to perform the task). A HAQ value .1.25 reflects severe disease.
Radiological examination TMJ Green-sensitive X-ray films measuring 24630 cm (AGFAH) were used in the current study. Two images were taken for each TMJ with linear tomograph technique, one with open mouth and the other in maximal occlusion. Evaluation was performed using the Rohlin–Petersson method,13,17 modified by Larsen, which rates TMJ according to erosion severity as follows (Fig. 1): grade 15normal conditions: welldefined condylar and glenoid shape, with convex cortical; grade 25slightly abnormal: minor changes such as osteophytes, crushing, and sclerosis. Uncertain findings are also included in this grade; grade 35moderate destructive abnormality: local erosions and changes; grade 45severe destructive abnormality: extensive erosions in the condyle and the temporal bone, with medial and lateral extension; and grade 55mutilating abnormalities: total erosion of the condyle with loss of articular surfaces and ankylosis. Hands The carpal technique was used with a focus/film distance of 1 m, without angulation, with the focal point in the metacarpo-phalangeal joint. Comparative films from both hands were requested. The radiological evaluation was performed with the Larsen method,13 which includes the assessment of the 2nd, 3rd, 4th and 5th metacarpo-phalangeal joints, second, third, fourth, and fifth proximal interphalangeal joints, and the carpus, considered in four sections: two upper sections and two lower ones. A value was adjudicated to each joint according to the abnormalities observed, which were summed to obtain the total value for each hand. Larsen grades were as follows: grade 05intact articular shape and preserved interarticular space; grade 15mild erosions lower than 1 mm, and slight reduction of the articular space, juxtaarticular osteoporosis, or soft tissue swelling; grade 25articular space reduced by less than 50%, with preserved joint and erosion greater than 1 mm; grade 35articular space reduced by more than 50% and marked erosion; grade 45osteal ankylosis with partially preserved bone shape; grade 55osteal ankylosis without preserved bone shape. VOL .
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Figure 1 Normal TMJ and hand, and assessment of right hand and right TMJ in a RA patient having the disease for a duration of 15 years. A reduction of the articular space in the carpus, with collapses and ankylosis, can be observed in the hand, together with reduced osteal shape in the second, third, fourth, and fifth metacarpophalangeal joints. A reduced osteal shape with ankylosis can also be observed in the second, third, fourth, and fifth proximal joints. The TMJ presents a grade 3 severity on the Rohlin–Petersson scale, including moderately destructive abnormality, erosive changes of the anterior and posterior condylar surface, and reduction of the articular space.
Statistical analysis
Frequency and presentation of TMJ pathologies
The statistical measures of position and dispersion were calculated for each variable. A retrospective case–control observational design was implemented to evaluate the prevalence of TMJ pathologies in 100 patients with RA. For statistical analysis, the authors calculated statistical measures of dispersion and position for each variable. The test used to compare differences in percentages is the test of differences in proportions (P). To study the strength of associations between two variables, the authors used the Pearson correlation coefficient (R).
The RA sample included 95 patients (84% female and 16% male) with a mean age of 45 years and a mean disease duration of 10.5 years (range: 2–39 years). Based on the questionnaire, headache was present in 53 (58%) of the RA patients, masticatory muscle pain was present in 57%, shoulder pain was present in 56%, and forefront pain was present in 33%. The clinical examination disclosed impaired mouth opening in 40 cases (42.1%) and reduced mouth opening (less than 40 mm) in 67 (71%), which was significantly more frequent than in the control group (13.6% with reduced opening).
Results RA severity
Table 1 Sample distribution
The severity of RA in the 95 patients, and the results of the clinical, radiological, and laboratory evaluations are shown in Tables 1 and 2.
Variable Sex (female/male) Age, mean (range) RA duration, mean (range)
84%/16% 45 years (24–74 years) 10.5 years (2–39 years)
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Table 2 Comparison between groups using the proportion differences test (P)* Frequency and presentation of stomatognathic system findings Clinical findings
Questionnaire
Impaired mouth opening Impaired mastication Dental pieces lost (less than 20 remaining) Reduced maximal opening Blocked opening from reduced maximal opening group ERS (mm/h) Headache TMJ pain TMJ clicks TMJ crepitations Masticatory muscles pain Shoulders pain Forefront pain
RA (n595)
Control (n522)
P
32 23 56 40 67
3 (14%) 3 (14%) 0% 3 (13.6%) 0%
0.073 0.508 … 0.000 0.000
2 (9.1%) 8 (36.36)% Control (n544) 1 (2.27%) 1 (2.27%) 8 (18.18%) 2% 0 0
0.004 H/S 0.339(N/S) P* 0.000 (H/S) 0.000 (H/S) 0,0065 (N/S) 0.000 (H/S)
(33.68%) (23.24%) (58.94%) (42.1%) (71%)
43 (45.3%) 53 (58%) AR (n5190) 57.89% (109) 110 (55.78%) 80 (42.10%) 57% 56% 33%
(N/S) (N/S) (H/S) (H/S)
Note: *P: proportion differences test. RA, rheumatoid arthritis; TMJ, temporomandibular joint; H/S, highly significant association; S, significant association; N/S, nonsignificant association.
Other abnormalities detected were clicks, which were significantly more frequent in RA joints than in those of the control group (55.78% versus 2.27%, P50.000), and crepitations, which were detected in 80 TMJs (42.10%, not significantly different from the control group; P50.065). Pain was present in 109 TMJs from RA patients (57.89%), being unilateral in 82 cases (75.24%) and bilateral in 27 (24.77%). The Das 28 index revealed a high disease activity in 31.34% of RA patients, moderate activity in 47.51%, and low activity in 14.15%. In contrast, it indicated low disease activity in all the individuals from the control group. The HAQ yielded values between 0 and 0.5 in 43% of the cases, and between 0.5 and 1 in 21%, thus showing that RA patients did not exhibit an important functional impairment. In the control group, the HAQ value was 0 in 95% of the cases, and only one individual presented a value of 1.1. ESR values (upper reference value 30 mm) were increased in 40.85% of RA patients, while 59% of controls had values between 11 and 20 mm. Radiological studies revealed that 168 (88.42%) of the 190 TMJs evaluated had some degree of erosion, according to the Rholin–Petersson classification, together with condylar destruction, deformity or integrity loss (Table 3). Twelve joints per hand were evaluated, so in 95 patients, 1140 joints per side, or a total of 2280 joints were evaluated. Some degree of erosion was detected in almost 80% of these joints.
Table 3 Classification of TMJ erosion degree according to the Rholin–Petersson score TMJ erosion stages according to Rholin–Petersson TMJ classification (n5190)
Control (n544)
P
Grade 0 Grade 1 Grade 2 Grade 3 Grade 4 Grade 5 Unclassified
42 (95.45%) 2 (4.54%) 0 0 0 0 0
0.000 H/S 0.005 H/S … … … … …
22 (11.57%) 34 (17.89%) 49 (25.78%) 45 (23.68%) 31 (16.31%) 8 (4.21%) 1(0.52%)
Note: *P: proportion differences test. H/S, highly significant association; N/S, non-significant association.
in the hands, according to Larsen classification. In contrast, TMJ erosions were not significantly associated with Das 28 scores (r50.28), HAQ values (r50.07), or ESR values (r50.07) (Fig. 2 and Table 5).
Association analysis A highly significant association (r50.62) was found between TMJ erosions and radiological findings 34
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Figure 2 Association between Larsen scores and Rholin– Petersson scores (Pearson correlation coefficient r).
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Table 4 Classification of hand erosion degree according to the score of Larsen Erosion degree in hands according to Larsen
Affected hand joints in RA patients (n)
Affected hand joints in RA patients (%)
Affected hand joints in control group (n)
Affected hand joints in control group (%)
P*
Grade 0 Grade 1 Grade 2 Grade 3 Grade 4 Grade 5 Unclassified
457 588 462 366 190 193 24
20.04 25.78 20.26 16.05 8.33 9.46 1.05
503 25 0 0 0 0 0
95.26 4.73 0 0 0 0 0
P50.000 H/S P50.002 H/S … … … … …
Note: *P: proportion differences test. H/S, highly significant association.
Table 5 Association between the Rholin–Petersson scores and the Larsen scores, Das 28, HAQ, and ESR values ATM
Larsen
ERS
HAQ
DAS 28
r Sign.
0.62 AS
0.07 NS
0.07 NS
0.28 NS
To study the strength of associations between two variables, the Pearson’s correlation coefficient r, not P was used.
Discussion The majority of individuals from the two groups included in the present study were females. Among RA patients, the proportion of females was 83%, which is in agreement with previous reports on the gender distribution of RA.18–23 Headache was present in 58% of RA patients, in concordance with the study by Koh et al.,24 who found this complaint in 47.5% of 80 patients with RA evaluated for temporomandibular disorders. TMJ pain was detected in 57.89% of the RA patients included in the present study, which agrees with the findings of Kallemberg and Scuttelari,18,25 who concluded that RA patients are prone to develop TMJ pain at different times, according to RA flares. Previous studies by Wort et al.26 mention infrequent TMJ pain among patients with rheumatic diseases, and attribute these complaints to myalgias, fibrositis, and ligaments pain, which is in contrast to the findings in the current study, in which 57.89% of the RA patients had TMJ pain. Given the presence of bone erosions and the close up of osteal insertions, it is expected that pain in the articular region is due to RA rather than to other conditions of myogenic origin. TMJ clicks were detected in 55.78% of the RA patients at the time of examination. Similarly, EttalaYlitalo et al.27 found TMJ clicks in 53.3% of 60 RA patients, and Ozcan et al.28 found this type of sounds in 48.8% of 43 RA patients. Owing to bone lesions in TMJ and the diminished space for the articular disc, an osteal
friction on a soft tissue of TMJ may exist, producing the clicks detected in patients. The percentages of patients having clicks and crepitations were higher in this study than those reported by Koh et al.,24 who found these sounds in 21.3% and 27.5%, respectively. The presence of crepitations is frequent in inflammatory and degenerative disorders, as revealed by other studies.12,20,29,30 Crepitations were prevalent in the RA patients included in the present study, being unilateral in 26.31% of the cases and bilateral in 15.78%, yielding a total prevalence of 42.10%. According to Hajati and Wiese,31,32 crepitation is a clinical sign of condylar surface destruction in chronic arthritis, and correlates with radiological signs of erosion in TMJ and hands, potentially constituting a predictor of bone erosion. From the RA patients evaluated, 58.94% presented less than 20 teeth (most of them being posterior teeth — first or second molars), which differs markedly from the control group in which 77.27% of the patients had more than 20 teeth. This may be related to the positive association between periodontal disease and RA reported by Mercado et al. and Garib and Qaradaxi.33,34 The maximal mouth opening was diminished in 42.5% of the RA patients included in the current study, in line with the findings of Angyal et al.35 and Yilmaz et al.,36 and the mouth opening was restricted in 67 cases (71%). Some type of erosion was detected in 85.77% of the joints assessed. This is coincident with several previous studies37–39 that included radiological evaluation of TMJ. However, not all the evaluation tests considered the bone surface, the free space available for the disc, and the presence of osteophytes and facets as the Rholin–Petersson method does. In agreement with the report by Tsiklaki,40 the radiological examination had an important role in the diagnosis of TMJ pathologies. No significant association was found between HAQ, DAS, or ESR values and the TMJ findings,
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thus showing that TMJ lesions do not correlate with disease activity, so that TMJ may be affected in varying degrees during the acute stage of RA. This may be due to the fact that Das 28 and HAQ do not consider functions of the stomatognathic system such as eating, speaking, or yawning. As these functions are among the ones that are impaired in RA patients, their inclusion in the HAQ may help detect some incapacity at joint or dental levels. Future studies should modify this questionnaire by including some of these variables, thus contributing to the early detection of TMJ impairments in RA patients. The most relevant radiological findings were erosion of the condylar surface, subcortical sclerosis of the condyle, and diminution of the space for the articular disc. Erosions in the hands were significantly associated with radiological findings in TMJ (r50.62) using the Rholin–Petersson method. To the best of the authors’ knowledge, this study is the first to establish an association between both variables. This allows the rheumatologist to predict that patients with bone erosions in the hands will likely have some type of TMJ lesion, making necessary the referral to an odontologist for treatment of the joint affected by RA.
Conclusions A highly significant association was found in the present study between headache and TMJ erosions. TMJ pain was present in 57.89% of RA patients, clicks were detected in 55.78%, crepitations were found in 42.10%, TMJ pain at rest was reported by 53.51%, and 58.94% of the patients had fewer than 20 teeth, thus lacking dental support. Mouth opening was diminished in 42.1% of the patients and was blocked in 71%. Based on radiological evaluation of TMJ, 25.8%, 23.68%, and 16.31% of the patients were classified into groups 2, 3, and 4 of Rholin–Petersson, respectively. According to carpal Rx films, 25.78%, 20.26%, and 16.05% of the RA patients were classified into grade 1, 2 and 3 of Larsen, respectively, whereas 96.02% of individuals from the control group were classified into group 0. A highly significant association was found between TMJ erosions graded according to the method of Rholin–Petersson and the carpal radiological findings classified according to the method of Larsen. In contrast, no association was found between TMJ erosions and HAQ, DAS, or ESR values. Signs of TMJ pathologies should be systematically sought in RA patients to allow their early detection, since clinical symptoms frequently attributed to muscle contracture can be caused by such pathologies. The authors propose to start such assessment 36
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from the early stages of RA, as this may facilitate the diagnosis and treatment of TMJ disorders. All rheumatologic patients should be screened. The maintenance of an adequate dental support may avoid an aggravating factor for the progressive TMJ damage during RA. The collaborative work between rheumatologists and odontologists may lead to an early diagnosis of TMJ disorders, allowing the design of combined therapeutic strategies aimed at minimizing the damage to an important joint with indispensable functions for human life.
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