Accepted Manuscript Surface electromyography and magnetic resonance imaging of the masticatory muscles in patients with arthrogenous temporomandibular disorders Gianluigi Lodetti , Giuseppe Marano , Paola Fontana , Gianluca M. Tartaglia , Claudia Maria de Felício , Elia Biganzoli , Chiarella Sforza PII:
S2212-4403(14)00473-8
DOI:
10.1016/j.oooo.2014.05.005
Reference:
OOOO 919
To appear in:
Oral Surgery, Oral Medicine, Oral Pathology and Oral Radiology
Received Date: 7 February 2014 Revised Date:
6 May 2014
Accepted Date: 7 May 2014
Please cite this article as: Lodetti G, Marano G, Fontana P, Tartaglia GM, de Felício CM, Biganzoli E, Sforza C, Surface electromyography and magnetic resonance imaging of the masticatory muscles in patients with arthrogenous temporomandibular disorders, Oral Surgery, Oral Medicine, Oral Pathology and Oral Radiology (2014), doi: 10.1016/j.oooo.2014.05.005. This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
ACCEPTED MANUSCRIPT Surface electromyography and magnetic resonance imaging of the masticatory muscles in patients with arthrogenous temporomandibular disorders. 1,2
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Gianluigi Lodetti , Giuseppe Marano , Paola Fontana , Gianluca M. Tartaglia , 4
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Claudia Maria de Felício , Elia Biganzoli , and Chiarella Sforza 1
Dipartimento di Scienze Biomediche per la Salute, Functional Anatomy Research Center (FARC),
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Laboratorio di Anatomia Funzionale dell'Apparato Stomatognatico (LAFAS), Facoltà di Medicina e Chirurgia, Università degli Studi di Milano, Milano, Italy 2
Dipartimento di Specialità Medico Chirurgiche, Scienze Radiologiche e Sanità Pubblica, Clinica
Odontoiatrica, Università degli Studi di Brescia, Brescia, Italy 3
Maccacaro”, Università degli Studi di Milano, Milano, Italy 4
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Dipartimento di Scienze Cliniche e di Comunità, Istituto di Statistica Medica e Biometria “G.A.
Departamento de Oftalmologia, Otorrinolaringologia e Cirurgia de Cabeça e Pescoço, Faculdade de
Medicina, Ribeirão Preto, Universidade de São Paulo, Brasil 5
Bioinformatica, Milano, Italy
MS submitted to Oral
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Fondazione IRCCS Istituto Nazionale dei Tumori, Struttura Complessa di Statistica Medica, Biometria e
surgery, oral medicine, oral pathology and oral radiology on 20 May 2014
Running title: EMG and RM in arthrogenous TMD
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Number of tables: 3 Number of figures: 3
Correspondence Prof. Chiarella Sforza
via Mangiagalli 31 I-20133 MILANO – ITALY
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Dipartimento di Scienze Biomediche per la Salute
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TEL. +39 – 02 503 15407 FAX +39 – 02 503 15387
E-mail address: [email protected]
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ACCEPTED MANUSCRIPT ABSTRACT The purpose of this study was to verify the characteristics of surface electromyography (sEMG) of masticatory muscles in different temporomandibular disorder (TMD) patients. Twenty-four TMD patients were categorized according to the RDC/TMD; Magnetic Resonance Images (MRI) classified patients with disk displacement (DD, mean age 22 years, SD 5; M/F: 3/6), and osteoarthrosis and/or disk displacement (OA,
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mean age 37 years, SD 10; M/F: 4/11); sEMG was performed according to a standardized protocol. The MRI score was significantly correlated to torque coefficient (r=0.57), temporalis (r=0.85) and masseter (r=0.46) muscle standardized symmetry. The discriminating ability of subject age and EMG scores in
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separating the two groups was assessed by ROC analysis. Each of the EMG scores showed a significant ability in discriminating between osteoarthrosis and disc displacement.
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The recording of the masticatory muscle function through sEMG can be a first diagnostic approach to TMD patients, reserving MRI assessment to selected cases.
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Key-words: temporomandibular joint disorder; sEMG; RMI; osteoarthrosis; disc dislocation; ROC analysis.
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ACCEPTED MANUSCRIPT INTRODUCTION Temporomandibular disorders (TMD) are among the most studied chronic orofacial pain conditions. Dworkin et al. (1992, 1990) and Suvinen et al. (2009) estimate that 7% of the general population are in need of treatment. In their systematic review, Dahlström and Carlsson (2010) underline the impact of this pathology on the Oral health-related quality of life (OHRQoL). The twelve studies that fulfilled the inclusion criteria of
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their review demonstrate a negative impact on the quality of life in patients diagnosed with a TMD. Although the epidemiologic prevalence of TMD in women (Le Resche, 1997; Mobilio et al., 2011), no sex differences in the clinical aspects of the disease were reported.A muscular diagnosis of TMD, arthralgia or disk
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displacement without reduction were associated with a more important impact on OHRQoL than disk displacement with reduction. The articles selected in that review show that OHRQoL is influenced principally by pain and not by functional limitation of the jaw.
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This aspect concords with the findings reported by Greenspan et al. (2011) in large case-control study: TMD patients are more sensitive to many experimental noxious stimuli at extracranial body sites than control persons.
An accurate anamnesis and a clinical examination supplemented with imaging are considered the gold standard for diagnosis of a pathology not completely understood yet (Cairns, 2010; Douglas et al., 2010;
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Epker et al., 1999; Tartaglia et al., 2011). In order to use uniform assessment criteria, in 1992 Dworkin and LeResche introduced the Research Diagnostic Criteria for Temporomandibular Disorders (RDC/TMD). This system has two assessment components. Axis I, a clinical and radiographic assessment, is designed to
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differentiate myofascial pain, disc displacement, and arthralgia, arthritis, and arthrosis. Axis II evaluates psychologic status and pain-related disability.
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Some authors discussed the relation between RDC/TMD and image findings provided by magnetic resonance imaging (MRI). Galhardo et al. (2013a) reported that the use in clinical practice of RDC/TMD is limited because of the high rate of false-positive results.Robinson de Senna et al. (2009) assert that the type of dysfunction and severity of alterations on the imaging exams were not related to the severity of pain or mandibular range of motion assessed with RDC/TMD. In a recent review, Koh et al. (2009) report that there is no evidence between clinical findings and MRI. Park et al. (2012) suggested the use of MRI when clinical examinations cannot predict the true position of the disc. Other investigators (Kurita et al., 2000; Ren et al., 1995; Westesson et al., 1985) state that the presence of skeletal changes is a sign of progress of disease, because it occurs in the joints with advanced internal derangement and it is associated with the duration of the symptoms.
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ACCEPTED MANUSCRIPT MRI provides information concerning joint morphology and inflammation that cannot be discerned through clinical examination (Park et al., 2012), but it has major limitations because of the high operating costs. MRI requires highly qualified technical staff, long times of image acquisition, and expensive medical equipment. Different protocols have been developed to objectively record the dysfunction present and to supplement the diagnosis of TMD as surface electromyography (sEMG). sEMG analyses the masticatory muscles activity
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through an objective and quantitative record (Castroflorio et al., 2008; De Felicio et al. 2009; Forrester et al., 2010; Santana-Mora et al., 2009; Suvinen et al., 2009).
Tartaglia et al. (2008) used the quantitative sEMG characteristics of the masticatory muscles of TMD patients
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to allow a differentiation among different diagnostic categories defined according to the RDC/TMD. In particular, it was possible to differentiate between healthy control subjects and arthrogenous and psycogenous patients, where a significant reduction in the standardized muscular activity was found.
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More recently, De Felicio et al. showed significant correlations among sEMG findings, orofacial myofunctional status and TMD severity, showing that the larger deviations from sEMG reference values were found in the patients with the worse clinical findings (De Felicio et al., 2012). Apparently, in no previous investigations, the objective characteristics of masticatory muscles were compared among subgroups of patients categorized according to the MRI interpretation. In the present
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study, a group of TMD patients were categorized according to both RDC/TMD and MRI in patients with disk displacement, osteoarthrosis and/or disk displacement. The quantitative sEMG characteristics of their masticatory muscles were analyzed. We wanted to see if patients in the different groups had some objective
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differences in the sEMG characteristics of their masticatory muscles during standardized teeth clenching. Patient data were also compared to those collected in two control subject groups without muscular or
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temporomandibular joint (TMJ) alterations.
MATERIALS AND METHODS Patients
In year 2010, 100 patients with pain in the pre-auricular area, movement limitation and joint sounds during the functional excursions of the jaw were referred to the Dental Clinic of the University of Brescia for TMJ treatment. All subjects were visited by a dentist, and their clinical history was gathered according to the Research Diagnostic Criteria for TMD (RDC/TMD) (Dworkin et al., 1992; Epker et al., 1999). Among the patients, those who presented arthrogenous TMD according to on the RDC/TMD, axis I, groups II and III, were selected to undergo bilateral high resolution MRI scans of TMJs, and a surface EMG analysis of their
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ACCEPTED MANUSCRIPT masticatory muscles. All patients had a long lasting TMD (duration of symptoms longer than 6 months) (Tartaglia et al., 2011). Additional inclusion criteria were: pain to one or both joints (larger than 4 on a 1-no pain- to 10-the largest possible pain- Visual Analogue Scale) during mastication, limitation during opening (maximal non forced opening < 30 mm) or during left and right excursion or protrusion (< 7 mm), at last one molar maxillary-
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mandibular contact per dental hemiarch.
Exclusion criteria were: presence of congenital craniofacial anomalies and/or systemic disease, dental pain, periodontal problems, craniofacial and cervical trauma and surgery, mono o bilateral posterior edentulism,
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current orthodontic treatment.
According to the inclusion and exclusion criteria, 24 patients were selected (17 women and 7 men, age range 14-60 years, mean 31 years, SD 11). According to the MRI examination protocol (see below), patients
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were subdivided in group A (15 patients: 11 women and 4 men, age range 26-60 years, mean 37, SD 10), patients with osteoarthrosis (Figure 1), and group B (9 patients: 6 women, 3 men, age range 14-29 years, mean 22, SD 5), patients with a damage limited to the soft tissues (mono or bilateral disc dislocation) (figure 2).
Group A was significantly older than group B, so we recruited two different control groups: a “young” control
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group (CB; 19 subjects, 9 men and 10 women, age range 20-35 years, mean 23 years, SD 2) and an “old” control group (CA; 19 subjects, 5 men and 14 women, age range 26-71 years, mean 37 years, SD 12). All control subjects were submitted to clinical evaluation according to the RDC/TMD and to sEMG
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examination. All subjects were healthy, with no history of any musculoskeletal problems, selected for the study according to the following inclusion criteria: no multiple teeth prostheses; up to three single tooth
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prostheses on natural teeth; a minimum of 14 occluding pairs of teeth; bilateral molar and canine Angle Class I occlusion; no periodontal problems; no craniofacial and cervical trauma and surgery; no TMD disorders and no current orthodontic treatment. All subjects gave their informed consent to all the clinical, MRI and EMG procedures that were a part of the treatment currently offered. Consent was also obtained from the parents/ legal guardians of the patients younger than 18 years. The study protocol was approved by the local ethic committee. All procedures were not-invasive, not dangerous, and did not provoke pain or discomfort to the subjects, who were free to stop their examinations in any moment. All procedures were conducted according to Helsinki Declaration.
Experimental protocol
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ACCEPTED MANUSCRIPT For all patients MRI and sEMG analyses were performed on the same day. Magnetic resonance imaging - MRI scans were performed on a 1.5 Tesla MR unit (Magneton SP 4000; Siemens, Erlangen, Germany). Parasagittal (perpendicular to the long axis of the mandiblar condyles) and coronal 3-mm slice views, with the mouth in the closed, partially open, and open positions by using a mouth prop, were obtained.
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For all patients, the scanning parameters were: 2D-Flash Sequence 35°; time of repetition=400ms; time of echo=12 ms; 256x256 matrix; number of excitations=4.
The MRI images were independently assessed by two radiologists for condylar-fossa morphology, disc
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displacement and presence of joint effusion. If their evaluations differed, the images were rechecked by the two radiologists together, and only those findings on which both radiologists concurred were recorded. Condylar bone changes were categorized as osteophyte formation and bone marrow edema; soft tissue
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morphology allowed for categorization of the joints as normal disc position, anterior disc displacement with reduction, anterior disc displacement without reduction, thinning, cracking or warping disc (Kurita et al., 2000; Westesson et al. 1985).
For each patient, MRI scores were calculated for both joints. One point was given to anterior disc displacement with reduction, one other point for fluid joint effusion, two points were given for anterior disc
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displacement without reduction, three points for osteophyte formation, and five points for thinning, cracking or warping disc. The values were doubled in the presence of bone marrow edema (Kurita et al., 2000; Westesson et al. 1985; Amaral et al., 2013).
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No information from the MRI interpretation was available to the dentist who performed the EMG assessment.
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EMG recordings - In all patients and control subjects, sEMG of the right and left masseter and anterior temporal muscles was performed during maximum voluntary teeth clenching (MVC) (Forrester et al., 2010; Ferrario et al., 2000). Two sets of tests were made in all subjects: a standardization recording (clench on cotton rolls) and a test recording (clench in intercuspal position) (Sforza et al., 2009). sEMG was made by an operator who was blind to the actual TMJ diagnosis. Numerical codes were used, and group assessment was made only at the end of data collection. To standardize the EMG potentials of the analyzed muscles with tooth contact, two 10-mm thick cotton rolls were positioned on the mandibular second premolars/ first molars of each patient, and a 5-s MVC was recorded. EMG activity was subsequently recorded during a MVC in intercuspal position. For both recordings, the patient was invited to clench as hard as possible, and to maintain the same level of
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ACCEPTED MANUSCRIPT contraction for 5 s; during test performance, the patients were verbally encouraged to perform at their best. All patients repeated the MVC test three times. The tests were explained and shown to the patients, who practiced before actual data acquisition. For all tests, the patients sat with their head unsupported and were asked to maintain a natural erect position. To avoid any fatigue’s effect, a rest period of at least 3 minutes was allowed between each test. In
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all patients, clenching did not provoke additional muscular/ articular pain in both conditions (MVC on cotton rolls/ occlusal surfaces).
Disposable, pre-gelled, silver/silver chloride bipolar surface electrodes (diameter 10 mm, interelectrode
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distance 21±1 mm) were positioned according to the recommendations of SENIAM (Surface EMG for NonInvasive Assessment of Muscles, Hermens et al., 2000). In brief, the electrodes were fixed on the skin in correspondence of the muscular bellies parallel to muscular fibers: anterior temporal: vertically along the
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anterior margin of the muscle (about on the coronal suture); masseter: parallel to the muscular fibers, with the upper pole of the electrode at the intersection between the tragus-labial commissura and the exocanthion-gonion lines. A disposable reference electrode was applied to the forehead. EMG activity was recorded using a computerized instrument (Freely, De Götzen srl; Legnano, Milano, Italy). The analog EMG signal was amplified (gain 150, peak-to-peak input range from 0 to 2,000 µV) using a
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differential amplifier with a high common mode rejection ratio (CMRR = 105 dB in the range 0-60 Hz, input impedance 10 GΩ), digitized (12 b resolution, 2230 Hz A/D sampling frequency), and digitally filtered (highpass filter set at 30 Hz, low-pass filter set at 400 Hz, band-stop for common 50-60 Hz noise). Using the EMA
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software (De Götzen srl; Legnano, Milano, Italy), the signals were averaged over 25 ms, with muscle activity assessed as the root mean square (RMS) of the amplitude (unit: µV). EMG signals were recorded for further
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analysis.
EMG data analysis - For all tests, the 3-s period with the most constant RMS EMG signal was automatically selected by the software and used for all subsequent analyses, that were automatically performed by the computer software. For each subject, the EMG potentials of the analyzed muscles recorded during the MVC tests were expressed as percent of the mean potential recorded during the standardization test (MVC on the cotton rolls) (Ferrario et al., 2006), unit: µV/µV x 100. All subsequent calculations were made with the standardized potentials. For each subject, the values obtained in the three MVC tests were averaged.
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ACCEPTED MANUSCRIPT A set of standardized EMG indices were computed (Ferrario et al., 2006). To assess muscle symmetry, within each subject the EMG waves of paired (right and left, masseter and temporalis) muscles were compared by computing a percentage overlapping coefficient (POC, unit: %). POC is an index of the symmetric distribution of muscular activity as determined by occlusion; it ranges between 0 and 100%: when two paired muscles contract with perfect symmetry, a POC of 100% is obtained.
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Because an unbalanced contractile activity of contralateral temporalis and masseter muscles, for instance left masseter and right temporalis, might give rise to a potential lateral displacing component, the Torque Coefficient (TC, unit %) was calculated. This index ranges between 0% (complete presence of lateral
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displacing force) to 100% (no lateral displacing force) (Ferrario et al., 2006).
To individuate the most prevalent pair of masticatory muscles, the activity index (Ac, unit %) was computed as the percentage ratio of the difference between the mean temporalis and masseter standardized
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potentials, and the sum of the same standardized potentials (Ferrario et al. 2000, Forrester et al. 2010). Ac is positive (up to 100%) when the masseter muscle standardized potentials are larger than the temporalis muscles ones, negative (up to –100%) when the temporalis muscles potentials are larger, and null when they are equal.
The mean (masseter and temporalis) total standardized muscle activities (unit: µV/µV·s %) were computed
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as the integrated areas of the EMG potentials over time (Ferrario et al., 2010). Reproducibility of surface EMG measurements was tested both within the same session and after 6 months,
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finding no systematic differences and limited random errors (De Felicio et al., 2009).
Statistical analysis - Descriptive statistics (mean and SD) of all variables (gender, age, EMG indices and MRI
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score) were computed for each group (A, patients with osteoarthrosis; B, patients with a damage limited to the soft tissues; CA and CB, control subjects). Differences in the distributions of gender were assessed by Chi-square test. A p < 0.05 was considered as statistically significant. Each EMG variable was standardized against the values obtained in the healthy control subjects by calculating absolute (sign less) z scores (patient value minus mean reference value divided by the SD of the reference group) (Sforza et al. 2009). The association of the standardized EMG variables with the MRI score was evaluated through scatter plots and correlation coefficients, namely: Pearson’s linear correlation coefficient r, and Spearman’s monotone correlation coefficient rho. Since no substantial deviation from linearity emerged, only Pearson coefficients were reported.
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ACCEPTED MANUSCRIPT The discriminating ability of subject age and z scores in separating group A and group B was assessed by ROC analysis, both for single and multiple variables. For the latter case, diagnostic indexes (one for each EMG variable) were obtained by multiple logistic regression models where age and z scores were included as independent variables. The Area Under the ROC curve (AUROC) and its 95% confidence interval (C.I.) were calculated by DeLong method (Pepe, 2003).
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A further aim was to evaluate the discriminating ability of EMG variables accounting for age. To this end, the differences between the AUROC of age and AUROCs of the diagnostic indexes above were assessed by Z tests, and by confidence intervals obtained through bootstrap resampling methods (non parametric, with
All analyses were carried out with R software (R Core Team, 2013).
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RESULTS
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2000 bootstrap samples for each estimate, Pepe, 2003).
Table 1 shows the distribution of gender, age, sEMG and MRI data of the analyzed patients and control subjects. The distribution of gender among the four groups (two patient groups and two control groups) was not significantly different (χ2=2.378; 3 degrees of freedom, P = 0.498).
EMG data in the patient groups were standardized using the control group data, and z-scores were
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calculated. Concerning the association of age and z scores of the EMG indices with the MRI score, the correlation coefficient was quite high for POC temporalis (r=0.85, with 95% C.I., 0.69-0.93), and moderately high for TC (r=0.57, 95% C.I., 0.21-0.79) and POC masseter (r=0.46, 95% C.I., 0.07-0.73), while for age and
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the other z scores the coefficient was not significant at the level of 5% (Table 2 and Figure 3). Each of the z scores showed a significant, moderately high ability in discriminating between osteoarthrosis
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(group A) and damaged soft tissues (group B), with AUROCs ranging from 0.73 to 0.79 (Table 3A). Subject age showed a high discriminating ability with an AUROC of 0.91. However, according to the confidence intervals of the estimated AUROC values, there is no evidence to state that the discriminating ability of age is different with respect to EMG variables. The subsequent analyses yielded better AUROC values for the diagnostic indexes including age and each EMG variable (Table 3A). Therefore, the additional diagnostic contribution of EMG variables accounting for the effect of age was assessed by a statistical testing procedure. In a first step the difference was assessed by asymptotic Z tests, which yielded no statistical evidence of an increment of discriminating performance. Since the limitations due the sample size, a less formal assessment was also performed through the
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ACCEPTED MANUSCRIPT Bootstrap estimation approach. The results reported in Table 3B show that standardized TC may have a significant contribution to the diagnosis after accounting for age: its confidence interval does not include 0.
DISCUSSION
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The diagnosis of TMD is usually performed by clinical investigation combined with imaging techniques. MRI of the TMJ has been indicated as gold standard in diagnosis because it offers accurate information about joint morphology and alterations. The need of imaging techniques (MRI and Computed Tomography) is still controversial because of high operating costs, thus leaving a key role to clinical assessments and history
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taking (Park et al., 2012). Conversely, some authors (Fujiwara et al., 2013; Galhardo et al., 2013b) reported that TMJ abnormalities cannot be reliably assessed by clinical examination only. The current scientific
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guidelines suggest that practitioners should image only if there is a reasonable expectation that additional information will influence a patient’s treatment approach (Riberio-Rotta et al., 2011). In order to support the clinical findings with some quantitative functional data, different protocols have been developed to objectively record the dysfunction. In particular, sEMG analysis of the masticatory muscles is currently a part of patient assessment in dentistry (Ferrario et al., 2006). This method provides quantitative
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data on the function of superficial muscles without invasive or dangerous procedures and without discomfort to the patient. As a matter of fact, sEMG is not universally considered a useful tool for TMD diagnosis (Dworkin et al., 1990, 1992): if well-standardized methods were not used, the problems in EMG reliability and
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validity hinder its clinical validity (de Luca et al., 1996). Among the major problems there are technical artefacts (instrumental noise); differences due to facial type, age, sex, thickness of subcutaneous fat (Dworkin et al., 1992; Klasser et al., 2006), cross talk from different muscles. Therefore, a correct EMG
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assessment should be performed only with standardized (normalized) potentials, thus removing most of biological and technical noise (Castroflorio et al., 2005; Manfredini et al., 2012). When well-standardized protocols are used, surface EMG of the head (masticatory) muscles has been reported to be an effective method for the functional assessment of the stomatognathic system (Hugger et al., 2008; Forrester et al., 2010; Tartaglia et al., 2011), with a good repeatability (Ferrario et al., 2006; Kogawa et al., 2006) to unravel some aspects of jaw elevator muscles functioning (Manfredini et al., 2012). In the current study, the standardization recording was obtained without dental contact by making the subjects clench on two cotton rolls positioned on mandibular molars (Ferrario et al., 2006). Standardized EMG indices recorded in MVC had already been used as a diagnostic test to differentiate between patients
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ACCEPTED MANUSCRIPT with TMD and neck disorders (Hermens et al., 2000), among different nonoverlapping RDC/TMD subgroups (Ferrario et al., 2006), and between patients with long lasting TMD and healthy subjects (Tartaglia et al., 2011). De Felicio et al. (2012) discriminated TMD patients from healthy women through clinical and instrumental examinations. The authors found that the Orofacial Myofunctional Evaluation using Scores Protocol, together
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with a sEMG assessment of masticatory muscles, provides information about the components and functions of the stomatognathic system (De Felicio et al., 2008, 2010).
The detection of the relationships between the various diagnostic tools is one of the fundamental steps for
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the assessment of their validity and clinical performance. For this reason we investigated the relationship between MRI assessment and sEMG analysis, that has been apparently neglected in the scientific literature so far.
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In the present study, healthy subjects and TMD patients, categorized in patients with osteoarthrosis and patients with a damage limited to the soft tissues through MRI, were submitted to sEMG, and the quantitative characteristics of their masticatory muscles were analyzed.
MRI characteristics allowed a clear differentiation between the two groups, that had also significant differences in their sEMG alterations relative to control healthy subjects matched for age and sex.
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Additionally, sEMG variables allowed to discriminate between the two patient groups as defined by MRI examination. For this reason, the objective recording of the masticatory muscle function and dysfunction through sEMG can be a first diagnostic approach to TMD patients. Surface standardized EMG is not
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invasive, low cost, and it can be made directly in the dental office, without the necessity of sending the patient to specialized diagnostic centres (Castroflorio et al., 2005; Ferrario et al., 2006; Forrester et al., 2010;
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Santana-Mora et al., 2009; Tartaglia et al., 2008). The male: female ratio of the current study was approximately 1 man to 2–3 women. Indeed, TMD is more frequently found in women than in men (Ferrario et al., 2002). Nevertheless, the sex distribution did not significantly differ between the two patients groups. Previous investigations found no significant effects of sex on normalized EMG indices (Ferrario et al., 2007), when the effect of age was ruled out. Age was significantly different between groups (patients with osteoarthrosis were significantly older than patients with a damage limited to the soft tissues and control subjects); the effect was statistically controlled using zscores computed from control groups of comparable age. The age differences between patients with osteoarthrosis and patients with a damage limited to the soft tissues can be explained with the clinical findings of TMD. Condylar and eminence bone changes might
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ACCEPTED MANUSCRIPT reflect the details of the progression of TMJ osteoarthrosis, that occurs predominantly in the joints with advanced internal derangement (Ren et al., 1995). However, the present study suffers of some limitations. First of all the small sample of patients with TMD related to the difficulty to find subjects with a chronic TMJ degeneration who respected the inclusion/ exclusion criteria. Moreover, MRI was not performed in the subjects of the control groups: we recruited the
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healthy subjects following standardized clinical protocols. Indeed, Tasaki et al. (1996) reported a range of asymptomatic internal derangements in up to 33% of the joints, but these numbers are probably connected with an incorrect interpretation of MRI (Provenzano et al., 2012). On the other side, we believe not ethically
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acceptable to vast resources in expensive instrumental examinations if it is not strictly necessary (RibeiroRotta et al., 2011).
The current data suggest that sEMG in controlled protocols can be an important diagnostic tool in TMD
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patients, providing additional information that cannot be obtained by clinical assessment and history. Indeed, notwithstanding a significant mean age difference between the two groups, there is some overlap between them. For instance, four patients of group A (27% of the analyzed patients) had an age (20, 26, 26 and 27 years) well included in the range of group B. A diagnostic classification based only on age would not include these subject in the arthrosis group, and this is ethically not acceptable. In perspective, TMJ arthrosis in a
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young person is a pathology with high costs in terms of sufferance and money (Currie, 2011; Honda et al., 2011). An early diagnosis could reduce the gravity of the problems, providing a more conservative therapy with generally a good patient response (Sahlström et al., 2013). An anterior disc displacement is in fact an
2006; Amaral et al., 2013).
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intracapsular dysfunction that leads to degenerative changes in the disc and joint surfaces (Orhan et al.,
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The exclusive use of clinical criteria to detect these subjects is also problematic because pain in the TMJ and mandibular area is better tolerated by younger than by older patients (Mobilio et al., 2011), and it could indicate different types of diseases (Fujiwara et al., 2013). The EMG assessment enabled to classify the gravity of the pathology guiding the clinician on the opportunity to prescribe new diagnostic exams or different therapeutic approaches. In conclusion, the results of the current investigation support the importance of clinical and instrumental examinations of the stomatognathic system; all of them provide useful information for diagnosis. The use of sEMG may be proposed for a first screening of patients with TMD, submitting to MRI only those that have the largest discrepancies from the reference values. Furthermore, understanding how evaluation methods are related is an important step toward a better diagnosis and a more effective treatment planning.
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ACCEPTED MANUSCRIPT CONFLICT OF INTEREST The authors declare no conflict of interest.
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ACCEPTED MANUSCRIPT Dworkin SF, Huggins KH, LeResche L, Von Korff M, Howard J, Truelove E, Sommers E. Epidemiology of signs and symptoms in temporomandibular disorders: clinical signs in cases and controls. J Am Dent Assoc. 1990; 120: 273-281. Dworkin SF, LeResche L. Research diagnostic criteria for temporomandibular disorders: review, criteria, examinations and specifications, critique. J Craniomandib Disord. 1992; 6: 301-355.
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ACCEPTED MANUSCRIPT Honda K, Yasukawa Y, Fujiwara M, Abe T, Urade M. Causes of persistent joint pain after arthrocentesis of temporomandibular joint. J Oral Maxillofac Surg. 2011; 69: 2311-2315. Hugger A, Hugger S, Schindler HJ. Surface electromyography of the masticatory muscles for application in dental practice. Current evidence and future developments. Int J Comput Dent. 2008; 11: 81-106.
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Klasser GD, Okeson JP. The clinical usefulness of surface electromyography in the diagnosis and treatment
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Kurita H, Ohtsuka A, Kobayashi H, Kurashina K. Is the morphology of the articular eminence of the temporomandibular joint a predisposing factor for disc displacement? Dentomaxillofac Radiol. 2000; 29:
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Manfredini D, Castroflorio T, Perinetti G, Guarda-Nardini L. Dental occlusion, body posture and temporomandibular disorders: where we are now and where we are heading for. J Oral Rehabil. 2012;
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Mobilio N, Casetta I, Cesnik E, Catapano S. Prevalence of self-reported symptoms related to
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temporomandibular disorders in an Italian population. J Oral Rehabil. 2011; 38: 884-890. Murray GM, Peck CC. Orofacial pain and jaw muscle activity: a new model. J Orofac Pain. 2007; 21: 263278.
Naeije M, Kalaykova S, Visscher CM, Lobbezoo F. Evaluation of the Research Diagnostic Criteria for Temporomandibular Disorders for the recognition of an anterior disc displacement with reduction. J Orofac Pain. 2009; 23: 303-311. Orhan K, Nishiyama H, Tadashi S, Murakami S, Furukawa S. Comparison of altered signal intensity, position, and morphology of the TMJ disc in MR images corrected for variations in surface coil sensitivity. Oral Surg Oral Med Oral Pathol Oral Radiol Endod. 2006; 101: 515-522.
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ACCEPTED MANUSCRIPT Park JW, Song HH, Roh HS, Kim YK, Lee JY. Correlation between clinical diagnosis based on RDC/TMD and MRI findings of TMJ internal derangement. Int J Oral Maxillofac Surg. 2012; 41: 103-108. Pepe MS. The statistical evaluation of medical tests for classification and prediction. Oxford. Oxford University Press. 2003 Provenzano Mde M, Chilvarquer I, Fenyo-Pereira M. How should the articular disk position be analyzed? J
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Ribeiro-Rotta RF, Marques KD, Pacheco MJ, Leles CR. Do computed tomography and magnetic resonance imaging add to temporomandibular joint disorder treatment? A systematic review of diagnostic efficacy. J Oral Rehabil. 2011; 38: 120-135.
Robinson de Senna B, Marques LS, França JP, Ramos-Jorge ML, Pereira LJ. Condyle-disk-fossa position and relationship to clinical signs and symptoms of temporomandibular disorders in women. Oral Surg
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Oral Med Oral Pathol Oral Radiol Endod. 2009; 108: 117-124. Sahlström LE, Ekberg EC, List T, Petersson A, Eriksson L. Lavage treatment of painful jaw movements at disc displacement without reduction. A randomized controlled trial in a short-term perspective. Int J Oral
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Santana-Mora U, Cudeiro J, Mora-Bermúdez MJ, Rilo-Pousa B, Ferreira-Pinho JC, Otero-Cepeda JL,
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Santana-Penín U. Changes in EMG activity during clenching in chronic pain patients with unilateral temporomandibular disorders. J Electromyogr Kinesiol. 2009; 19: 543-549. Sforza C, Tartaglia GM, Lovecchio N, Ugolini A, Monteverdi R, Giannì AB, Ferrario VF. Mandibular movements at maximum mouth opening and EMG activity of masticatory and neck muscles in patients rehabilitated after a mandibular condyle fracture. J Craniomaxillofac Surg. 2009; 37: 327-333. Suvinen TI, Malmberg J, Forster C, Kemppainen P. Postural and dynamic masseter and anterior temporalis muscle EMG repeatability in serial assessments. J Oral Rehabil. 2009; 36: 814-820. Tartaglia GM, Lodetti G, Paiva G, De Felicio CM, Sforza C. Surface electromyographic assessment of patients with long lasting temporomandibular joint disorder pain. J Electromyogr Kinesiol. 2011; 21: 659664.
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ACCEPTED MANUSCRIPT Tartaglia GM, Moreira Rodrigues da Silva MA, Bottini S, Sforza C, Ferrario VF. Masticatory muscle activity during maximum voluntary clench in different research diagnostic criteria for temporomandibular disorders (RDC/TMD) groups. Man Ther. 2008; 13: 434-440. Tasaki MM, Westesson PL, Isberg AM, Ren YF, Tallents RH. Classification and prevalence of temporomandibular joint disk displacement in patients and symptom-free volunteers. Am J Orthod
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Dentofacial Orthop. 1996; 109: 249-262.
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Surg Oral Med Oral Pathol. 1985; 59: 220-224.
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ACCEPTED MANUSCRIPT Table 1. Descriptive statistics of the analyzed patients and control subjects. Group A
unit
Group B
N
Mean 15
Mean 19
SD
Men
N
4
3
9
5
Women
N
11
6
10
14
Age
Y
37
10
22
5
22
POC masseter
%
79.5
12.0
85.8
4.3
84.3
POC temporalis
%
73.5
14.9
86.4
5.9
85.0
TC
%
87.4
5.4
90.5
3.3
89.2
Activity index
%
1.3
23.4
-2.6
9.5
µV/µV·s %
112.9
58.2
103.2
11.9
5
Mean 19
37
SD
12.0
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SD
3.8
86.7
1.9
2.8
86.7
2.2
1.9
90.6
1.2
-6.3
12.6
-3.2
4.7
109.5
36
104.1
29.6
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Mean 9
Group CA
Total
Activity standardized
SD
Group CA
Table 2. Correlation with MRI score.
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MRI score N 8.53 4.20 2.22 0.97 ----Group A, patients with osteoarthrosis; group B, patients with a damage limited to the soft tissues; groups CA and CB, control subjects
95% C.I.
p-value
Age
0.37
(-0.04, 0.67)
0.07374
POC masseter
0.46
( 0.07, 0.73)
0.02483
POC temporalis
0.85
( 0.69, 0.93)
S2212-4403(14)00473-8
DOI:
10.1016/j.oooo.2014.05.005
Reference:
OOOO 919
To appear in:
Oral Surgery, Oral Medicine, Oral Pathology and Oral Radiology
Received Date: 7 February 2014 Revised Date:
6 May 2014
Accepted Date: 7 May 2014
Please cite this article as: Lodetti G, Marano G, Fontana P, Tartaglia GM, de Felício CM, Biganzoli E, Sforza C, Surface electromyography and magnetic resonance imaging of the masticatory muscles in patients with arthrogenous temporomandibular disorders, Oral Surgery, Oral Medicine, Oral Pathology and Oral Radiology (2014), doi: 10.1016/j.oooo.2014.05.005. This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
ACCEPTED MANUSCRIPT Surface electromyography and magnetic resonance imaging of the masticatory muscles in patients with arthrogenous temporomandibular disorders. 1,2
3
2
1
Gianluigi Lodetti , Giuseppe Marano , Paola Fontana , Gianluca M. Tartaglia , 4
3,5
1
Claudia Maria de Felício , Elia Biganzoli , and Chiarella Sforza 1
Dipartimento di Scienze Biomediche per la Salute, Functional Anatomy Research Center (FARC),
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Laboratorio di Anatomia Funzionale dell'Apparato Stomatognatico (LAFAS), Facoltà di Medicina e Chirurgia, Università degli Studi di Milano, Milano, Italy 2
Dipartimento di Specialità Medico Chirurgiche, Scienze Radiologiche e Sanità Pubblica, Clinica
Odontoiatrica, Università degli Studi di Brescia, Brescia, Italy 3
Maccacaro”, Università degli Studi di Milano, Milano, Italy 4
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Dipartimento di Scienze Cliniche e di Comunità, Istituto di Statistica Medica e Biometria “G.A.
Departamento de Oftalmologia, Otorrinolaringologia e Cirurgia de Cabeça e Pescoço, Faculdade de
Medicina, Ribeirão Preto, Universidade de São Paulo, Brasil 5
Bioinformatica, Milano, Italy
MS submitted to Oral
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Fondazione IRCCS Istituto Nazionale dei Tumori, Struttura Complessa di Statistica Medica, Biometria e
surgery, oral medicine, oral pathology and oral radiology on 20 May 2014
Running title: EMG and RM in arthrogenous TMD
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Number of tables: 3 Number of figures: 3
Correspondence Prof. Chiarella Sforza
via Mangiagalli 31 I-20133 MILANO – ITALY
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Dipartimento di Scienze Biomediche per la Salute
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TEL. +39 – 02 503 15407 FAX +39 – 02 503 15387
E-mail address: [email protected]
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ACCEPTED MANUSCRIPT ABSTRACT The purpose of this study was to verify the characteristics of surface electromyography (sEMG) of masticatory muscles in different temporomandibular disorder (TMD) patients. Twenty-four TMD patients were categorized according to the RDC/TMD; Magnetic Resonance Images (MRI) classified patients with disk displacement (DD, mean age 22 years, SD 5; M/F: 3/6), and osteoarthrosis and/or disk displacement (OA,
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mean age 37 years, SD 10; M/F: 4/11); sEMG was performed according to a standardized protocol. The MRI score was significantly correlated to torque coefficient (r=0.57), temporalis (r=0.85) and masseter (r=0.46) muscle standardized symmetry. The discriminating ability of subject age and EMG scores in
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separating the two groups was assessed by ROC analysis. Each of the EMG scores showed a significant ability in discriminating between osteoarthrosis and disc displacement.
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The recording of the masticatory muscle function through sEMG can be a first diagnostic approach to TMD patients, reserving MRI assessment to selected cases.
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Key-words: temporomandibular joint disorder; sEMG; RMI; osteoarthrosis; disc dislocation; ROC analysis.
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ACCEPTED MANUSCRIPT INTRODUCTION Temporomandibular disorders (TMD) are among the most studied chronic orofacial pain conditions. Dworkin et al. (1992, 1990) and Suvinen et al. (2009) estimate that 7% of the general population are in need of treatment. In their systematic review, Dahlström and Carlsson (2010) underline the impact of this pathology on the Oral health-related quality of life (OHRQoL). The twelve studies that fulfilled the inclusion criteria of
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their review demonstrate a negative impact on the quality of life in patients diagnosed with a TMD. Although the epidemiologic prevalence of TMD in women (Le Resche, 1997; Mobilio et al., 2011), no sex differences in the clinical aspects of the disease were reported.A muscular diagnosis of TMD, arthralgia or disk
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displacement without reduction were associated with a more important impact on OHRQoL than disk displacement with reduction. The articles selected in that review show that OHRQoL is influenced principally by pain and not by functional limitation of the jaw.
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This aspect concords with the findings reported by Greenspan et al. (2011) in large case-control study: TMD patients are more sensitive to many experimental noxious stimuli at extracranial body sites than control persons.
An accurate anamnesis and a clinical examination supplemented with imaging are considered the gold standard for diagnosis of a pathology not completely understood yet (Cairns, 2010; Douglas et al., 2010;
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Epker et al., 1999; Tartaglia et al., 2011). In order to use uniform assessment criteria, in 1992 Dworkin and LeResche introduced the Research Diagnostic Criteria for Temporomandibular Disorders (RDC/TMD). This system has two assessment components. Axis I, a clinical and radiographic assessment, is designed to
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differentiate myofascial pain, disc displacement, and arthralgia, arthritis, and arthrosis. Axis II evaluates psychologic status and pain-related disability.
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Some authors discussed the relation between RDC/TMD and image findings provided by magnetic resonance imaging (MRI). Galhardo et al. (2013a) reported that the use in clinical practice of RDC/TMD is limited because of the high rate of false-positive results.Robinson de Senna et al. (2009) assert that the type of dysfunction and severity of alterations on the imaging exams were not related to the severity of pain or mandibular range of motion assessed with RDC/TMD. In a recent review, Koh et al. (2009) report that there is no evidence between clinical findings and MRI. Park et al. (2012) suggested the use of MRI when clinical examinations cannot predict the true position of the disc. Other investigators (Kurita et al., 2000; Ren et al., 1995; Westesson et al., 1985) state that the presence of skeletal changes is a sign of progress of disease, because it occurs in the joints with advanced internal derangement and it is associated with the duration of the symptoms.
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ACCEPTED MANUSCRIPT MRI provides information concerning joint morphology and inflammation that cannot be discerned through clinical examination (Park et al., 2012), but it has major limitations because of the high operating costs. MRI requires highly qualified technical staff, long times of image acquisition, and expensive medical equipment. Different protocols have been developed to objectively record the dysfunction present and to supplement the diagnosis of TMD as surface electromyography (sEMG). sEMG analyses the masticatory muscles activity
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through an objective and quantitative record (Castroflorio et al., 2008; De Felicio et al. 2009; Forrester et al., 2010; Santana-Mora et al., 2009; Suvinen et al., 2009).
Tartaglia et al. (2008) used the quantitative sEMG characteristics of the masticatory muscles of TMD patients
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to allow a differentiation among different diagnostic categories defined according to the RDC/TMD. In particular, it was possible to differentiate between healthy control subjects and arthrogenous and psycogenous patients, where a significant reduction in the standardized muscular activity was found.
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More recently, De Felicio et al. showed significant correlations among sEMG findings, orofacial myofunctional status and TMD severity, showing that the larger deviations from sEMG reference values were found in the patients with the worse clinical findings (De Felicio et al., 2012). Apparently, in no previous investigations, the objective characteristics of masticatory muscles were compared among subgroups of patients categorized according to the MRI interpretation. In the present
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study, a group of TMD patients were categorized according to both RDC/TMD and MRI in patients with disk displacement, osteoarthrosis and/or disk displacement. The quantitative sEMG characteristics of their masticatory muscles were analyzed. We wanted to see if patients in the different groups had some objective
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differences in the sEMG characteristics of their masticatory muscles during standardized teeth clenching. Patient data were also compared to those collected in two control subject groups without muscular or
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temporomandibular joint (TMJ) alterations.
MATERIALS AND METHODS Patients
In year 2010, 100 patients with pain in the pre-auricular area, movement limitation and joint sounds during the functional excursions of the jaw were referred to the Dental Clinic of the University of Brescia for TMJ treatment. All subjects were visited by a dentist, and their clinical history was gathered according to the Research Diagnostic Criteria for TMD (RDC/TMD) (Dworkin et al., 1992; Epker et al., 1999). Among the patients, those who presented arthrogenous TMD according to on the RDC/TMD, axis I, groups II and III, were selected to undergo bilateral high resolution MRI scans of TMJs, and a surface EMG analysis of their
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ACCEPTED MANUSCRIPT masticatory muscles. All patients had a long lasting TMD (duration of symptoms longer than 6 months) (Tartaglia et al., 2011). Additional inclusion criteria were: pain to one or both joints (larger than 4 on a 1-no pain- to 10-the largest possible pain- Visual Analogue Scale) during mastication, limitation during opening (maximal non forced opening < 30 mm) or during left and right excursion or protrusion (< 7 mm), at last one molar maxillary-
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mandibular contact per dental hemiarch.
Exclusion criteria were: presence of congenital craniofacial anomalies and/or systemic disease, dental pain, periodontal problems, craniofacial and cervical trauma and surgery, mono o bilateral posterior edentulism,
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current orthodontic treatment.
According to the inclusion and exclusion criteria, 24 patients were selected (17 women and 7 men, age range 14-60 years, mean 31 years, SD 11). According to the MRI examination protocol (see below), patients
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were subdivided in group A (15 patients: 11 women and 4 men, age range 26-60 years, mean 37, SD 10), patients with osteoarthrosis (Figure 1), and group B (9 patients: 6 women, 3 men, age range 14-29 years, mean 22, SD 5), patients with a damage limited to the soft tissues (mono or bilateral disc dislocation) (figure 2).
Group A was significantly older than group B, so we recruited two different control groups: a “young” control
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group (CB; 19 subjects, 9 men and 10 women, age range 20-35 years, mean 23 years, SD 2) and an “old” control group (CA; 19 subjects, 5 men and 14 women, age range 26-71 years, mean 37 years, SD 12). All control subjects were submitted to clinical evaluation according to the RDC/TMD and to sEMG
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examination. All subjects were healthy, with no history of any musculoskeletal problems, selected for the study according to the following inclusion criteria: no multiple teeth prostheses; up to three single tooth
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prostheses on natural teeth; a minimum of 14 occluding pairs of teeth; bilateral molar and canine Angle Class I occlusion; no periodontal problems; no craniofacial and cervical trauma and surgery; no TMD disorders and no current orthodontic treatment. All subjects gave their informed consent to all the clinical, MRI and EMG procedures that were a part of the treatment currently offered. Consent was also obtained from the parents/ legal guardians of the patients younger than 18 years. The study protocol was approved by the local ethic committee. All procedures were not-invasive, not dangerous, and did not provoke pain or discomfort to the subjects, who were free to stop their examinations in any moment. All procedures were conducted according to Helsinki Declaration.
Experimental protocol
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ACCEPTED MANUSCRIPT For all patients MRI and sEMG analyses were performed on the same day. Magnetic resonance imaging - MRI scans were performed on a 1.5 Tesla MR unit (Magneton SP 4000; Siemens, Erlangen, Germany). Parasagittal (perpendicular to the long axis of the mandiblar condyles) and coronal 3-mm slice views, with the mouth in the closed, partially open, and open positions by using a mouth prop, were obtained.
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For all patients, the scanning parameters were: 2D-Flash Sequence 35°; time of repetition=400ms; time of echo=12 ms; 256x256 matrix; number of excitations=4.
The MRI images were independently assessed by two radiologists for condylar-fossa morphology, disc
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displacement and presence of joint effusion. If their evaluations differed, the images were rechecked by the two radiologists together, and only those findings on which both radiologists concurred were recorded. Condylar bone changes were categorized as osteophyte formation and bone marrow edema; soft tissue
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morphology allowed for categorization of the joints as normal disc position, anterior disc displacement with reduction, anterior disc displacement without reduction, thinning, cracking or warping disc (Kurita et al., 2000; Westesson et al. 1985).
For each patient, MRI scores were calculated for both joints. One point was given to anterior disc displacement with reduction, one other point for fluid joint effusion, two points were given for anterior disc
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displacement without reduction, three points for osteophyte formation, and five points for thinning, cracking or warping disc. The values were doubled in the presence of bone marrow edema (Kurita et al., 2000; Westesson et al. 1985; Amaral et al., 2013).
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No information from the MRI interpretation was available to the dentist who performed the EMG assessment.
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EMG recordings - In all patients and control subjects, sEMG of the right and left masseter and anterior temporal muscles was performed during maximum voluntary teeth clenching (MVC) (Forrester et al., 2010; Ferrario et al., 2000). Two sets of tests were made in all subjects: a standardization recording (clench on cotton rolls) and a test recording (clench in intercuspal position) (Sforza et al., 2009). sEMG was made by an operator who was blind to the actual TMJ diagnosis. Numerical codes were used, and group assessment was made only at the end of data collection. To standardize the EMG potentials of the analyzed muscles with tooth contact, two 10-mm thick cotton rolls were positioned on the mandibular second premolars/ first molars of each patient, and a 5-s MVC was recorded. EMG activity was subsequently recorded during a MVC in intercuspal position. For both recordings, the patient was invited to clench as hard as possible, and to maintain the same level of
6
ACCEPTED MANUSCRIPT contraction for 5 s; during test performance, the patients were verbally encouraged to perform at their best. All patients repeated the MVC test three times. The tests were explained and shown to the patients, who practiced before actual data acquisition. For all tests, the patients sat with their head unsupported and were asked to maintain a natural erect position. To avoid any fatigue’s effect, a rest period of at least 3 minutes was allowed between each test. In
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all patients, clenching did not provoke additional muscular/ articular pain in both conditions (MVC on cotton rolls/ occlusal surfaces).
Disposable, pre-gelled, silver/silver chloride bipolar surface electrodes (diameter 10 mm, interelectrode
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distance 21±1 mm) were positioned according to the recommendations of SENIAM (Surface EMG for NonInvasive Assessment of Muscles, Hermens et al., 2000). In brief, the electrodes were fixed on the skin in correspondence of the muscular bellies parallel to muscular fibers: anterior temporal: vertically along the
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anterior margin of the muscle (about on the coronal suture); masseter: parallel to the muscular fibers, with the upper pole of the electrode at the intersection between the tragus-labial commissura and the exocanthion-gonion lines. A disposable reference electrode was applied to the forehead. EMG activity was recorded using a computerized instrument (Freely, De Götzen srl; Legnano, Milano, Italy). The analog EMG signal was amplified (gain 150, peak-to-peak input range from 0 to 2,000 µV) using a
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differential amplifier with a high common mode rejection ratio (CMRR = 105 dB in the range 0-60 Hz, input impedance 10 GΩ), digitized (12 b resolution, 2230 Hz A/D sampling frequency), and digitally filtered (highpass filter set at 30 Hz, low-pass filter set at 400 Hz, band-stop for common 50-60 Hz noise). Using the EMA
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software (De Götzen srl; Legnano, Milano, Italy), the signals were averaged over 25 ms, with muscle activity assessed as the root mean square (RMS) of the amplitude (unit: µV). EMG signals were recorded for further
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analysis.
EMG data analysis - For all tests, the 3-s period with the most constant RMS EMG signal was automatically selected by the software and used for all subsequent analyses, that were automatically performed by the computer software. For each subject, the EMG potentials of the analyzed muscles recorded during the MVC tests were expressed as percent of the mean potential recorded during the standardization test (MVC on the cotton rolls) (Ferrario et al., 2006), unit: µV/µV x 100. All subsequent calculations were made with the standardized potentials. For each subject, the values obtained in the three MVC tests were averaged.
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ACCEPTED MANUSCRIPT A set of standardized EMG indices were computed (Ferrario et al., 2006). To assess muscle symmetry, within each subject the EMG waves of paired (right and left, masseter and temporalis) muscles were compared by computing a percentage overlapping coefficient (POC, unit: %). POC is an index of the symmetric distribution of muscular activity as determined by occlusion; it ranges between 0 and 100%: when two paired muscles contract with perfect symmetry, a POC of 100% is obtained.
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Because an unbalanced contractile activity of contralateral temporalis and masseter muscles, for instance left masseter and right temporalis, might give rise to a potential lateral displacing component, the Torque Coefficient (TC, unit %) was calculated. This index ranges between 0% (complete presence of lateral
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displacing force) to 100% (no lateral displacing force) (Ferrario et al., 2006).
To individuate the most prevalent pair of masticatory muscles, the activity index (Ac, unit %) was computed as the percentage ratio of the difference between the mean temporalis and masseter standardized
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potentials, and the sum of the same standardized potentials (Ferrario et al. 2000, Forrester et al. 2010). Ac is positive (up to 100%) when the masseter muscle standardized potentials are larger than the temporalis muscles ones, negative (up to –100%) when the temporalis muscles potentials are larger, and null when they are equal.
The mean (masseter and temporalis) total standardized muscle activities (unit: µV/µV·s %) were computed
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as the integrated areas of the EMG potentials over time (Ferrario et al., 2010). Reproducibility of surface EMG measurements was tested both within the same session and after 6 months,
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finding no systematic differences and limited random errors (De Felicio et al., 2009).
Statistical analysis - Descriptive statistics (mean and SD) of all variables (gender, age, EMG indices and MRI
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score) were computed for each group (A, patients with osteoarthrosis; B, patients with a damage limited to the soft tissues; CA and CB, control subjects). Differences in the distributions of gender were assessed by Chi-square test. A p < 0.05 was considered as statistically significant. Each EMG variable was standardized against the values obtained in the healthy control subjects by calculating absolute (sign less) z scores (patient value minus mean reference value divided by the SD of the reference group) (Sforza et al. 2009). The association of the standardized EMG variables with the MRI score was evaluated through scatter plots and correlation coefficients, namely: Pearson’s linear correlation coefficient r, and Spearman’s monotone correlation coefficient rho. Since no substantial deviation from linearity emerged, only Pearson coefficients were reported.
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ACCEPTED MANUSCRIPT The discriminating ability of subject age and z scores in separating group A and group B was assessed by ROC analysis, both for single and multiple variables. For the latter case, diagnostic indexes (one for each EMG variable) were obtained by multiple logistic regression models where age and z scores were included as independent variables. The Area Under the ROC curve (AUROC) and its 95% confidence interval (C.I.) were calculated by DeLong method (Pepe, 2003).
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A further aim was to evaluate the discriminating ability of EMG variables accounting for age. To this end, the differences between the AUROC of age and AUROCs of the diagnostic indexes above were assessed by Z tests, and by confidence intervals obtained through bootstrap resampling methods (non parametric, with
All analyses were carried out with R software (R Core Team, 2013).
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RESULTS
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2000 bootstrap samples for each estimate, Pepe, 2003).
Table 1 shows the distribution of gender, age, sEMG and MRI data of the analyzed patients and control subjects. The distribution of gender among the four groups (two patient groups and two control groups) was not significantly different (χ2=2.378; 3 degrees of freedom, P = 0.498).
EMG data in the patient groups were standardized using the control group data, and z-scores were
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calculated. Concerning the association of age and z scores of the EMG indices with the MRI score, the correlation coefficient was quite high for POC temporalis (r=0.85, with 95% C.I., 0.69-0.93), and moderately high for TC (r=0.57, 95% C.I., 0.21-0.79) and POC masseter (r=0.46, 95% C.I., 0.07-0.73), while for age and
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the other z scores the coefficient was not significant at the level of 5% (Table 2 and Figure 3). Each of the z scores showed a significant, moderately high ability in discriminating between osteoarthrosis
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(group A) and damaged soft tissues (group B), with AUROCs ranging from 0.73 to 0.79 (Table 3A). Subject age showed a high discriminating ability with an AUROC of 0.91. However, according to the confidence intervals of the estimated AUROC values, there is no evidence to state that the discriminating ability of age is different with respect to EMG variables. The subsequent analyses yielded better AUROC values for the diagnostic indexes including age and each EMG variable (Table 3A). Therefore, the additional diagnostic contribution of EMG variables accounting for the effect of age was assessed by a statistical testing procedure. In a first step the difference was assessed by asymptotic Z tests, which yielded no statistical evidence of an increment of discriminating performance. Since the limitations due the sample size, a less formal assessment was also performed through the
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ACCEPTED MANUSCRIPT Bootstrap estimation approach. The results reported in Table 3B show that standardized TC may have a significant contribution to the diagnosis after accounting for age: its confidence interval does not include 0.
DISCUSSION
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The diagnosis of TMD is usually performed by clinical investigation combined with imaging techniques. MRI of the TMJ has been indicated as gold standard in diagnosis because it offers accurate information about joint morphology and alterations. The need of imaging techniques (MRI and Computed Tomography) is still controversial because of high operating costs, thus leaving a key role to clinical assessments and history
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taking (Park et al., 2012). Conversely, some authors (Fujiwara et al., 2013; Galhardo et al., 2013b) reported that TMJ abnormalities cannot be reliably assessed by clinical examination only. The current scientific
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guidelines suggest that practitioners should image only if there is a reasonable expectation that additional information will influence a patient’s treatment approach (Riberio-Rotta et al., 2011). In order to support the clinical findings with some quantitative functional data, different protocols have been developed to objectively record the dysfunction. In particular, sEMG analysis of the masticatory muscles is currently a part of patient assessment in dentistry (Ferrario et al., 2006). This method provides quantitative
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data on the function of superficial muscles without invasive or dangerous procedures and without discomfort to the patient. As a matter of fact, sEMG is not universally considered a useful tool for TMD diagnosis (Dworkin et al., 1990, 1992): if well-standardized methods were not used, the problems in EMG reliability and
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validity hinder its clinical validity (de Luca et al., 1996). Among the major problems there are technical artefacts (instrumental noise); differences due to facial type, age, sex, thickness of subcutaneous fat (Dworkin et al., 1992; Klasser et al., 2006), cross talk from different muscles. Therefore, a correct EMG
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assessment should be performed only with standardized (normalized) potentials, thus removing most of biological and technical noise (Castroflorio et al., 2005; Manfredini et al., 2012). When well-standardized protocols are used, surface EMG of the head (masticatory) muscles has been reported to be an effective method for the functional assessment of the stomatognathic system (Hugger et al., 2008; Forrester et al., 2010; Tartaglia et al., 2011), with a good repeatability (Ferrario et al., 2006; Kogawa et al., 2006) to unravel some aspects of jaw elevator muscles functioning (Manfredini et al., 2012). In the current study, the standardization recording was obtained without dental contact by making the subjects clench on two cotton rolls positioned on mandibular molars (Ferrario et al., 2006). Standardized EMG indices recorded in MVC had already been used as a diagnostic test to differentiate between patients
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ACCEPTED MANUSCRIPT with TMD and neck disorders (Hermens et al., 2000), among different nonoverlapping RDC/TMD subgroups (Ferrario et al., 2006), and between patients with long lasting TMD and healthy subjects (Tartaglia et al., 2011). De Felicio et al. (2012) discriminated TMD patients from healthy women through clinical and instrumental examinations. The authors found that the Orofacial Myofunctional Evaluation using Scores Protocol, together
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with a sEMG assessment of masticatory muscles, provides information about the components and functions of the stomatognathic system (De Felicio et al., 2008, 2010).
The detection of the relationships between the various diagnostic tools is one of the fundamental steps for
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the assessment of their validity and clinical performance. For this reason we investigated the relationship between MRI assessment and sEMG analysis, that has been apparently neglected in the scientific literature so far.
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In the present study, healthy subjects and TMD patients, categorized in patients with osteoarthrosis and patients with a damage limited to the soft tissues through MRI, were submitted to sEMG, and the quantitative characteristics of their masticatory muscles were analyzed.
MRI characteristics allowed a clear differentiation between the two groups, that had also significant differences in their sEMG alterations relative to control healthy subjects matched for age and sex.
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Additionally, sEMG variables allowed to discriminate between the two patient groups as defined by MRI examination. For this reason, the objective recording of the masticatory muscle function and dysfunction through sEMG can be a first diagnostic approach to TMD patients. Surface standardized EMG is not
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invasive, low cost, and it can be made directly in the dental office, without the necessity of sending the patient to specialized diagnostic centres (Castroflorio et al., 2005; Ferrario et al., 2006; Forrester et al., 2010;
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Santana-Mora et al., 2009; Tartaglia et al., 2008). The male: female ratio of the current study was approximately 1 man to 2–3 women. Indeed, TMD is more frequently found in women than in men (Ferrario et al., 2002). Nevertheless, the sex distribution did not significantly differ between the two patients groups. Previous investigations found no significant effects of sex on normalized EMG indices (Ferrario et al., 2007), when the effect of age was ruled out. Age was significantly different between groups (patients with osteoarthrosis were significantly older than patients with a damage limited to the soft tissues and control subjects); the effect was statistically controlled using zscores computed from control groups of comparable age. The age differences between patients with osteoarthrosis and patients with a damage limited to the soft tissues can be explained with the clinical findings of TMD. Condylar and eminence bone changes might
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ACCEPTED MANUSCRIPT reflect the details of the progression of TMJ osteoarthrosis, that occurs predominantly in the joints with advanced internal derangement (Ren et al., 1995). However, the present study suffers of some limitations. First of all the small sample of patients with TMD related to the difficulty to find subjects with a chronic TMJ degeneration who respected the inclusion/ exclusion criteria. Moreover, MRI was not performed in the subjects of the control groups: we recruited the
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healthy subjects following standardized clinical protocols. Indeed, Tasaki et al. (1996) reported a range of asymptomatic internal derangements in up to 33% of the joints, but these numbers are probably connected with an incorrect interpretation of MRI (Provenzano et al., 2012). On the other side, we believe not ethically
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acceptable to vast resources in expensive instrumental examinations if it is not strictly necessary (RibeiroRotta et al., 2011).
The current data suggest that sEMG in controlled protocols can be an important diagnostic tool in TMD
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patients, providing additional information that cannot be obtained by clinical assessment and history. Indeed, notwithstanding a significant mean age difference between the two groups, there is some overlap between them. For instance, four patients of group A (27% of the analyzed patients) had an age (20, 26, 26 and 27 years) well included in the range of group B. A diagnostic classification based only on age would not include these subject in the arthrosis group, and this is ethically not acceptable. In perspective, TMJ arthrosis in a
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young person is a pathology with high costs in terms of sufferance and money (Currie, 2011; Honda et al., 2011). An early diagnosis could reduce the gravity of the problems, providing a more conservative therapy with generally a good patient response (Sahlström et al., 2013). An anterior disc displacement is in fact an
2006; Amaral et al., 2013).
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intracapsular dysfunction that leads to degenerative changes in the disc and joint surfaces (Orhan et al.,
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The exclusive use of clinical criteria to detect these subjects is also problematic because pain in the TMJ and mandibular area is better tolerated by younger than by older patients (Mobilio et al., 2011), and it could indicate different types of diseases (Fujiwara et al., 2013). The EMG assessment enabled to classify the gravity of the pathology guiding the clinician on the opportunity to prescribe new diagnostic exams or different therapeutic approaches. In conclusion, the results of the current investigation support the importance of clinical and instrumental examinations of the stomatognathic system; all of them provide useful information for diagnosis. The use of sEMG may be proposed for a first screening of patients with TMD, submitting to MRI only those that have the largest discrepancies from the reference values. Furthermore, understanding how evaluation methods are related is an important step toward a better diagnosis and a more effective treatment planning.
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ACCEPTED MANUSCRIPT CONFLICT OF INTEREST The authors declare no conflict of interest.
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ACCEPTED MANUSCRIPT Table 1. Descriptive statistics of the analyzed patients and control subjects. Group A
unit
Group B
N
Mean 15
Mean 19
SD
Men
N
4
3
9
5
Women
N
11
6
10
14
Age
Y
37
10
22
5
22
POC masseter
%
79.5
12.0
85.8
4.3
84.3
POC temporalis
%
73.5
14.9
86.4
5.9
85.0
TC
%
87.4
5.4
90.5
3.3
89.2
Activity index
%
1.3
23.4
-2.6
9.5
µV/µV·s %
112.9
58.2
103.2
11.9
5
Mean 19
37
SD
12.0
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SD
3.8
86.7
1.9
2.8
86.7
2.2
1.9
90.6
1.2
-6.3
12.6
-3.2
4.7
109.5
36
104.1
29.6
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Mean 9
Group CA
Total
Activity standardized
SD
Group CA
Table 2. Correlation with MRI score.
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MRI score N 8.53 4.20 2.22 0.97 ----Group A, patients with osteoarthrosis; group B, patients with a damage limited to the soft tissues; groups CA and CB, control subjects
95% C.I.
p-value
Age
0.37
(-0.04, 0.67)
0.07374
POC masseter
0.46
( 0.07, 0.73)
0.02483
POC temporalis
0.85
( 0.69, 0.93)
