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Evaluación Dirigida de La Articulación Temporomandibular en Pacientes Con Artritis Reumatoide PDF
Evaluación Dirigida de La Articulación Temporomandibular en Pacientes Con Artritis Reumatoide PDF
66:1804-1811, 2008
Purpose: This observational study was done to identify the signs and symptoms of temporomandibular
joint (TMJ) involvement in patients with rheumatoid arthritis (RA) and to assess the association between
these and quantitative measurements for the evaluation of rheumatologic disease.
Patients and Methods: The sample comprised 61 patients suffering from RA whose signs and
symptoms of TMJ were recorded by means of a questionnaire (scale of limited mandibular function) and
clinical measurements (pain during jaw movement, limitation of maximal mouth opening, joint sounds,
tenderness on TMJ palpation, tenderness on masticatory muscle palpation). These findings were corre-
lated with the quantitative measurements for evaluating RA: duration of the disease, positivity for
rheumatoid factor, Health Assessment Questionnaire (HAQ) score, number of edematous and painful
joints, and overall assessment of functional status.
Results: In terms of overall figures, 70.5% of the patients presented with at least 1 sign or symptom,
49.2% had at least 1 symptom, and 54.1% had at least 1 sign. The variable pain on movement was
associated with the number of painful joints and the overall assessment findings (P ⬍ .05). Sound on
movement was positively associated with the number of edematous joints (P ⫽ .0291). The scale of
limited mandibular function was statistically significantly correlated with 4 quantitative measurements
(P ⫽ .0283 to .0448). The variable pain on palpation of the masticatory muscles was associated with the
number of painful joints (P ⫽ .0023). Pain on palpation of the TMJ was statistically significantly
associated with the HAQ score (P ⫽ .0344) and with the number of painful joints (P ⫽ .0006).
Conclusion: A significant percentage of the patients with RA have signs and symptoms of TMJ
involvement, and the scale of limited mandibular function proved to be an important measurement tool.
© 2008 American Association of Oral and Maxillofacial Surgeons
J Oral Maxillofac Surg 66:1804-1811, 2008
Rheumatoid arthritis (RA) is a systemic inflammatory determined by genetic and environmental factors that
disease that manifests itself predominately in the sy- control the progression and pattern of inflammation.1
novial membrane of the joints in a symmetric fash- World epidemiologic data reveal that 1% of the
ion.1,2 RA is associated with a wide range of manifes- population suffers from RA.3-5 The female:male ratio
tations, from a temporarily limiting disease to a is 2.5:1, and the disease most frequently occurs be-
progressive chronic alteration, and may exhibit an tween ages 35 and 45 years.1 It is estimated that the
overt extra-articular clinical involvement in various survival of RA sufferers is 20% lower than in the
organs. The heterogeneity of these manifestations is general population, with mortality increasing in direct
*PhD Student, Oral and Maxillofacial Surgery, University of Per- 储Senior Resident, Oral and Maxillofacial Surgery, University of
nambuco, Recife, Brazil. Pernambuco, Recife, Brazil.
†Senior Lecturer and Director of the MSc and PhD Programs, Address correspondence and reprint requests to Dr Vasconce-
Oral and Maxillofacial Surgery, University of Pernambuco, Recife, los: Department of Oral and Maxillofacial Surgery, University of
Brazil. Pernambuco, 1650 Av General Newton Cavalcanti, 54753-220
‡Senior Lecturer, Department of Rheumatology, Federal Univer- Recife, PE, Brazil; e-mail: belmiro@pesquisador.cnpq.br
sity of Pernambuco, Recife, Brazil. © 2008 American Association of Oral and Maxillofacial Surgeons
§Senior Lecturer, Preventive and Social Dentistry, University of 0278-2391/08/6609-0005$34.00/0
Pernambuco, Recife, Brazil. doi:10.1016/j.joms.2007.08.037
1804
BESSA-NOGUEIRA ET AL 1805
proportion to the severity of the disease. Survival in ments: 1) an understanding of anatomic and physio-
the subgroup of RA patients with involvement in logical variables important for the diagnosis and 2)
more than 30 joints is 40% to 45% after 5 years, a the patient’s perception of his or her own limita-
figure corresponding to the survival of patients with tion.19
coronary disease.2 The present study was an observational investiga-
The progression of RA leads to an incapacity for tion aimed at identifying the signs and symptoms of
performing daily routine and professional activities, TMJ involvement in patients with RA and assessing
which has a significant negative socioeconomic im- their association with quantitative measurements for
pact on both patient and society as a whole. Early the assessment of RA.
diagnosis and immediate treatment are fundamental
for controlling the activity of the disease, with the aim
Patients and Methods
of preventing functional incapacity and irreversible
joint lesions.1,2,5,6 The study population comprised patients of both
Pain is an important determinant of the impact of genders and various social backgrounds suffering
RA, because it leads to limited joint movement and is from RA undergoing treatment at the Department of
associated with the onset of fatigue, asthenia, and Rheumatology, Pernambuco Federal University Hos-
morning stiffness. In general, the treatment of RA pital, between December 2003 and December 2004.
aims to improve joint function and stagnation of joint The following inclusion criteria were adopted: a diag-
damage and to prevent progression of the functional nosis of RA according to the American College of
incapacity and associated morbidity factors.1,2,5,6 Rheumatology’s 1987 criteria, no previous treatment
The involvement of the temporomandibular joint of any kind for TMJ involvement, and a sufficient
(TMJ) in patients with RA has been reported begin- number of teeth (or tooth prostheses) for obtaining
ning with the introduction of the term by Garrod in quantitative measurements of jaw movement. Any
1859.7 The literature demonstrates the importance of patient not wishing to participate in the study was
routinely assessing TMJ function to allow early detec- excluded. In compliance with resolutions on ethics in
tion of signs and symptoms of involvement and research involving humans, the project was approved
prompt intervention in cases requiring treatment.8 by the University of Pernambuco’s Ethics in Research
The likelihood of patients with RA developing TMJ Committee.
involvement is correlated with the severity and dura- The initial sample comprised 70 patients. Because 9
tion of the systemic disease.8-15 Epidemiologic studies of these lacked the required number of teeth for
have shown a frequency of TMJ involvement in RA verification of the data, the final sample comprised 61
ranging from 4.7% to 84%.11,12,14,15 This wide varia- patients (55 females and 6 males) ranging in age from
tion may be explained by differences in the popula- 24 to 76 years (mean, 44 years, 7 months).
tions studied or in the selection criteria used, or by The collection of data concerning RA was con-
inappropriate examination of the TMJ and adjacent ducted by a single examiner (R.V.B.N.) trained in the
musculature in patients with TMJ involvement.8,11,12 use of the assessment instruments used in the study.
The most common signs and symptoms of TMJ In the patient interview, data were collected on the
involvement are joint pain, edema, crepitation, and duration of RA, positivity for rheumatoid factor,
limited movement, all of which are associated with Health Assessment Questionnaire (HAQ) score, num-
jaw stiffness on mouth opening.14 The most common ber of edematous and painful joints, overall assess-
radiographic findings are erosion and flattening of the ment of the disease by the patient, and functional
head of the mandible and articular fossa and reduc- status. The HAQ is a self-assessment instrument
tion of the joint spaces,16 usually noticed 5 to 10 years through which patients assess the condition of their
after the onset of symptoms.15 joints. It comprises 20 questions related to difficulty
Research studies have demonstrated a correlation in performing daily activities and permits 4 possible
between the limitation of mouth opening and the answers: 0, no difficulty at all; 1, some difficulty; 2,
severity of RA.15 But this reduction in jaw movement great difficulty; and 3, incapacity. The scores of the
may present as an early or a late sign, sometimes answers are grouped and calculated, with a mean
giving a false impression of TMJ involvement.7 Such a score obtained to define the patient’s HAQ. The pa-
limitation may be caused by pain, the presence of tient’s final score is rated on a scale of 0 to 3, with 0
fibrous adhesions, or a more severe degeneration of indicating full ability to perform activities and 3 indi-
the TMJ.13,15,17,18 Thus, the measurement of maximal cating total incapacity.20
mouth opening as the sole assessment parameter does An overall assessment of the severity of the pa-
not appear to be reliable for analyzing TMJ function in tient’s signs and symptoms of RA was done using a
patients with RA.18 A targeted assessment of TMJ visual analog scale. The assessment of functional sta-
involvement in RA should include 2 fundamental ele- tus comprised 4 Classes (I to IV) that expressed the
1806 TMJ ASSESSMENT IN RHEUMATOID ARTHRITIS
Pain on Movement
Yes No Total
Study Variable n % n % n % P*
variable limitation of mandibular function revealed signs and symptoms demonstrated higher frequen-
the presence of at least 1 of its items in 63.9% of the cies. This difference is due to differences in the clas-
patients and the absence of all of the items in the sification and assessment of the signs and symptoms
remaining 36.1%. The variation ranged from 8.2% to in the various studies.7-11,13,17,23-25 Analysis of the age
50.8%, with the most frequently seen items being distribution of the patients showed that most (52.5%)
eating hard food (50.8%), chewing (39.3%), yawning were between 24 and 45 years old, a finding similar to
(34.4%), and smiling or laughing (24.6%). that reported by Goronzy and Weyand.1
The dependent and independent variables were The main features of the patients with RA in the
assessed inferentially in all of the associations. Tables sample were disease duration of more than 10 years
3 to 7 present only the results that exhibited statisti- (42.6%) and a positive rheumatoid factor (55.7%).
cally significant P values. These findings reflect the quantitative nature of the
assessment of RA; that is, 67.2% of the patients had an
HAQ score of 1 to 3; slightly less than 50% had 1 or
Discussion
more edematous joints (42.6%), more than 5 painful
Performing a targeted assessment of the TMJ in joints (45.9%), and an overall assessment ranging from
patients with RA requires special care owing to the 51 to 100 (42.6%); and 37.7% of the patients were
fact that a large percentage of these patients have able to perform activities relating to personal hygiene,
symptomatology. In terms of overall figures, 70.5% of with limitations for all other activities (Class III). The
the patients presented with at least 1 sign or symp- explanation for these findings, according to Laurindo
tom, 49.2% had at least 1 symptom, and 54.1% had at and Torigoe,5 is that more than 50% of the affected
least 1 sign. These findings are in agreement with individuals, after suffering from the disease for 10
other published studies showing that 33% to 66% of years, have difficulty performing their professional
the patients with RA have some sign or symptom of activities, and with the disease progression become
TMJ involvement; however, analysis of our patients’ unable to perform even their everyday activities, with
Table 5. ASSESSMENT OF THE SCALE OF LIMITATION OF MANDIBULAR FUNCTION ACCORDING TO THE METHOD
OF RA ASSESSMENT
Rhematoid factor
Positive 18 52.9 16 47.1 34 100.0 .0448†
Negative 21 77.8 6 22.2 27 100.0
Total group 39 63.9 22 36.1 61 100.0
HAQ
1 to 3 30 73.2 11 26.8 41 100.0 .0315†
0 to 1 9 45.0 11 55.0 20 100.0
Total group 39 63.9 22 36.1 61 100.0
Number of painful joints
More than 5 22 78.6 6 21.4 28 100.0 .0283†
Up to 5 17 51.5 16 48.5 33 100.0
Total group 39 63.9 22 36.1 61 100.0
Functional status
Class I 4 30.8 9 69.2 13 100.0 .0406‡
Class II 12 66.7 6 33.3 18 100.0
Class III 17 73.9 6 26.1 23 100.0
Class IV 6 85.7 1 14.3 7 100.0
Total group 39 63.9 22 36.1 61 100.0
*Significant association at a level of 5.0%.
†Using Pearson’s 2 test.
‡Using Fisher’s exact test.
Bessa-Nogueira et al. TMJ Assessment in Rheumatoid Arthritis. J Oral Maxillofac Surg 2008.
a resulting significant socioeconomic impact on both 49.2% of patients experienced pain on TMJ move-
the patients and society as a whole. Note that 60% to ment. Ogus,23 in a study of 62 patients with RA, found
90% of patients with RA develop the progressive form that 36% had pain on movement. In a series of 123
of the disease after 10 years26; in these cases, the patients with RA, Tegelberg and Kopp13 found that
relationship between inflammation and incapacity, 54% had pain on movement.
which was previously directly proportional to time, A small fraction of the patients had limited mandib-
comes to reflect the effect of the destruction of joints ular movement (14.8%), in agreement with previously
caused by the disease.27 reported findings.7,10-13,17,23-25 Nevertheless, there is
From the standpoint of the signs and symptoms of no uniformity regarding the normal patterns of move-
TMJ involvement, a coherence and harmony can be ment. Many of the previous studies followed what
seen in the distribution of the data collected, in which was proposed by Agerberg:28 maximal mouth open-
HAQ
1 to 3 22 53.7 19 76.3 41 100.0 .0344†
0 to 1 5 25.0 15 75.0 20 100.0
Total group 27 44.3 34 55.7 61 100.0
Number of painful joints
More than 5 19 67.9 9 32.1 28 100.0 .0006†
Up to 5 8 24.2 25 75.8 33 100.0
Total group 27 44.3 34 55.7 61 100.0
*Significant association at a level of 5.0%.
†Using Pearson’s 2 test.
Bessa-Nogueira et al. TMJ Assessment in Rheumatoid Arthritis. J Oral Maxillofac Surg 2008.
BESSA-NOGUEIRA ET AL 1809
Table 7. ASSESSMENT OF PAIN ON PALPATION OF THE MASTICATORY MUSCLES ACCORDING TO THE METHOD
OF RA ASSESSMENT
ing greater than 40 mm, right or left lateral move- results (Tables 3-7), we crossed these variables with 6
ments, and protrusion of the jaw greater than 7 mm. variables of TMJ analysis.22,29,30 Analysis of these tables
Sound on TMJ movement was found in 49.2% of the reveals an association between increased values of RA
patients, with a click in 19.7% and crepitation in measurement and a greater frequency of signs and
29.5%. These findings are in agreement with those of symptoms of TMJ involvement. The literature reports
other studies,8,10,16,23,24 demonstrating that TMJ that the likelihood of patients with RA developing symp-
sounds are a frequent finding and that the most com- toms in the TMJ is correlated with the severity and
mon sound is crepitation. Akerman et al24 studied the duration of the systemic disease; in other words, the
relationship between clinical and radiologic TMJ find- more severe the involvement, the greater the likelihood
ings in 101 patients with RA and found that 80% of the of it causing TMJ symptomatology.8-15
TMJs that presented with crepitation also exhibited Among all of the associations, rheumatoid factor
radiographic evidence of erosion; thus, crepitation was the only one that demonstrated divergent results;
can be considered a reliable predictive factor. How- that is, individuals who were negative for rheumatoid
ever, crepitation revealed a low sensibility in detect- factor reported a greater frequency of limited man-
ing joints with erosion, owing to the fact that half of dibular function (Table 5). The factor in question is an
the joints with evidence of erosion presented with indicator of the development of functional incapacity,
either a click or no sound at all. with the presence of extra-articular manifestations;
The analysis of palpation of the masticatory and thus, a positive rheumatoid factor suggests a poorer
TMJ muscles revealed that two thirds of the patients prognosis of RA. However, rheumatoid factor does
had no pain in the muscles, whereas 44.3% had pain not have the power to predict which joints will be
in the TMJ, with symmetrical involvement noted in most or least affected.31,32 On the other hand, the
29%. Ettala-Ylitalo et al,12 in their analysis of 60 pa- number of painful joints was the variable that most
tients, noted that 53.3% had pain on palpation of the frequently demonstrated a statistically significant as-
muscles. On the other hand, Koh et al8 analyzed 80 sociation with the dependent variables of the study
patients and found that only 16.2% had involvement (Tables 3, 5, 6, and 7).
of the musculature of mastication. Franks10 found that The variable pain on movement showed a statisti-
40% of the patients examined had pain on TMJ palpa- cally significant association with the number of pain-
tion. ful joints and with the overall assessment findings
The analysis of limitation of mandibular function (Table 3). This association leads us to believe that
demonstrated that the activities most affected were there is a strong likelihood that the patient, in report-
eating hard food (50.8%), chewing (39.3%), and yawn- ing pain in other body joints, will also refer to pain on
ing (34.4%). This may be accounted for by the results TMJ movement.
of Voog et al,6 who found a positive association be- The frequency of limited maximal mouth opening
tween pain during maximal mouth opening and pain was similar to that found in most of the previous
on TMJ palpation, correlated with difficulties in per- reports reviewed.7,10-13,17,23-25 According to Stegenga
forming everyday activities such as yawning and et al,19 maximal mouth opening is one of the most
mouth opening. We found that 44.3% of our patients frequently used variables in clinical trials. Nonethe-
experienced pain on maximal mouth opening and less, it fails to make a differential diagnosis, because
TMJ palpation. the limitation may exist for numerous reasons, includ-
In interpreting the inferential results, we used 7 vari- ing intra-articular and muscular factors. Restriction of
ables directly related to RA.26 To obtain the tables of intra-articular movements may be caused by obstruc-
1810 TMJ ASSESSMENT IN RHEUMATOID ARTHRITIS
23. Ogus H: Rheumatoid arthritis of the temporomandibular joint. 28. Agerberg G: Maximal mandibular movements in young men
Br J Oral Surg 12:275, 1975 and women. Sven Tandlak Tidskr 67:81, 1974
24. Akerman S, Kopp S, Nilner M, et al: Relationship between 29. Dworkin SF, Leresche L, Derouen T, et al: Assessing clinical
clinical and radiologic findings of the temporomandibular signs of temporomandibular disorders: Reliability of clinical
joint in rheumatoid arthritis. Oral Surg Oral Med Oral Pathol examiners. J Prosthet Dent 63:574, 1990
66:639, 1988 30. Kosminsky M, Lucena LBS, Siqueira JTT, et al: Adaptação cul-
25. Goupille P, Fouquet B, Goga D, et al: The temporomandibular tural do questionário research diagnostic criteria for temporo-
joint in rheumatoid arthritis: Correlations between clinical and mandibular disorders: Axis II para o Português. J Bras Clin
tomographic features. J Dent 21:141, 1993 Odontol Int 8:51, 2004
26. Pincus T: Assessment of long-term outcomes of rheumatoid 31. Vaz C, Cardoso A: Temas de Prática Médica: Artrite Re-
arthritis: How choices of measures and study designs may lead umatóide. Porto, Portugal, Medisa, 2000, p 48
to apparently different conclusions. Rheum Dis Clin North Am 32. Anderson RJ: Rheumatoid arthritis: Clinical and laboratory fea-
21:619, 1995 tures, in Klippel JH, Stone JH, Crofford L, et al (eds): Primer on
27. Kirwan JR: Conceptual issues in scoring radiographic progres- the Rheumatic Diseases (ed 12). (Atlanta, GA, Arthritis Foun-
sion in rheumatoid arthritis. J Rheumatol 26:720, 1992 dation, 2001, p 218