Statement of Clinical Relevance

Transcription

1 Vol. 117 No. 1 January 2014 Contingent electrical stimulation inhibits jaw muscle activity during sleep but not pain intensity or masticatory muscle pressure pain threshold in self-reported bruxers: a pilot study Paulo César R. Conti, PhD, a Juliana Stuginski-Barbosa, b Leonardo R. Bonjardim, PhD, c Simone Soares, PhD, d and Peter Svensson, PhD e University of São Paulo, Bauru, São Paulo, Brazil; and Aarhus University, Aarhus, Denmark Objective. This study investigated the effect of contingent electrical stimulation (CES) on present pain intensity (PI), pressure pain threshold (PPT), and electromyographic events per hour of sleep (EMG/h) on probable bruxers with masticatory myofascial pain. Study Design. The study enrolled 15 probable bruxers with masticatory myofascial pain in 3 phases: (1) baseline EMG/h recording, (2) biofeedback treatment using a CES paradigm (active group, n ¼ 7) or inactive device (control group, n ¼ 8), and (3) posttreatment EMG/h recording. PI and PPT were assessed after each phase. Analysis of variance models were used to compare results at a 5% significance level. Results. Patients in the active group had 35% lower EMG/h in P2 and 38.4% lower EMG/h in P3, when compared with baseline. There were no differences in PI or PPT levels at any phase. Conclusions. CES could reduce EMG activity associated with sleep bruxism in patients with masticatory myofascial pain but did not influence perceived pain. (Oral Surg Oral Med Oral Pathol Oral Radiol 2014;117:45-52) Sleep bruxism (SB) is defined as a repetitive jaw muscle activity characterized by clenching or grinding of the teeth or by bracing or thrusting of the mandible during sleep 1 and has been considered an important factor in the onset and perpetuation of pain in patients with temporomandibular disorders (TMDs). 2,3 The relationship between SB and TMDs, however, is still unclear because of several different methods to identify bruxism as well as the difficulty in clearly defining TMDs. When self-reported measures of SB and clinical signs of TMDs without clearly defined diagnostic criteria were used, a strong association could be found. 2,4 The relationship between SB and TMD pain became more complex owing to experimental studies as well as to more stringent criteria for detecting SB using polysomnography (PSG). 4 In PSG studies, patients with clinically assessed SB and masticatory This study was supported in part by Medotech A/S. Potential conflict of interest: P. Svensson is a paid consultant for Medotech A/S. a Professor, Department of Prosthodontics, Bauru School of Dentistry, University of São Paulo. b Doctorate Student, Department of Prosthodontics, Bauru School of Dentistry, University of São Paulo. c Professor, Departament of Biological Sciences, Bauru School of Dentistry, University of São Paulo. d Professor, Department of Prosthodontics, Bauru School of Dentistry, University of São Paulo. e Professor, Section of Clinical Oral Physiology, Department of Dentistry, Aarhus University; Center for Functionally Integrative Neuroscience (CFIN), MindLab, Aarhus University Hospital. Received for publication Apr 1, 2013; returned for revision Aug 8, 2013; accepted for publication Aug 15, Ó 2014 Elsevier Inc. All rights reserved /$ - see front matter muscle pain had 40% less jaw muscle activity (electromyographic events per hour of sleep, EMG/h) compared with bruxers without pain. 5 Indeed, sleep bruxers with low frequencies of orofacial activities, including jaw muscle activity, were more likely to complain of pain and fatigue of masticatory muscles. 6 Some studies also found no association between SB and masticatory myofascial pain 3,7 and suggested that SB may be a low-risk factor for masticatory myofascial pain. 8 Because of the difficulty in providing strong evidence for a direct relationship between SB and TMD pain, different interventions have been used with the aim to reduce jaw muscle activity during sleep and thereby decrease TMD pain. For example, occlusal appliances are believed to have a significant effect on self-reported pain and tenderness in patients with TMDs. 9 It has been found that occlusal appliances can, indeed, reduce jaw muscle activity during sleep, 10 but this inhibitory effect may occur only for a short period of time. 11 So the question still remains: Is a reduction in jaw muscle EMG activity directly related to a reduction in clinical TMD pain? Statement of Clinical Relevance This pilot study found that contingent electrical stimulation can reduce the number of electromyographic events per hour of sleep in self-reported bruxers but does not influence perceived pressure pain thresholds in these patients. 45

2 ORAL MEDICINE OOOO 46 Conti et al. January 2014 Jadidi et al. 12 found that a contingent electrical stimulation (CES) paradigm during sleep was associated with significant reduction in the number of detected EMG events in the anterior temporalis muscle. They used a novel feedback device that measured EMG activity mainly associated with tooth grinding or clenching during sleep (GrindCare, Medotech A/S, Herlev, Denmark). This device has 2 modes of operation: (1) measurement, that is, simple monitoring of the EMG activity of the anterior temporalis muscle, and (2) treatment, that is, emitting a nonpainful electrical pulse to the temporal region when EMG activity exceeds the individually determined threshold. 12 The inhibition of the jaw muscle activity by CES is thought to be based at least in part on an exteroceptive suppression reflex in the contracting jaw muscles. 12,13 Pain and tenderness in the jaw muscles are common findings in a population with TMDs. 14 A recent study found that CES not only reduced jaw muscle activity but also was able to decrease self-reported pain, restrictions on activities of daily life, and the number of painful muscles on palpation. 15 In contrast, other studies found a significant effect of CES in decreasing jaw muscle activity but found no changes in the number of painful muscles, maximum pain-free jaw opening, 13 or self-reported pain. 13,16 Pressure pain threshold (PPT) is defined as the minimum force applied that evokes a painful sensation. 17 LowerPPTshavebeenreportedinpatientswith TMDs compared with healthy controls Algometry is considered a reliable tool in the determination ofpptfordiagnosisaswellasforanalysisofthe efficacy of management strategies. 21,22 As can be seen, the real influence of CES on the levels of PPT in patients with myofascial TMD pain is still to be defined. The aim of this study was to investigate the effect of CES on present pain intensity (PI), PPT, and EMG activity in the anterior temporalis muscle of probable sleep bruxers with myofascial masticatory muscle pain. METHODS Study population The participants were recruited from patients referred to the Orofacial Pain Clinic, Bauru School of Dentistry, University of São Paulo, Bauru, São Paulo, Brazil. Participants were aged between 20 and 50 years, were classified with myofascial pain according to the Research Diagnostic Criteria for Temporomandibular Disorders (RDC/TMD), 23 and had familiar pain on palpation in the masseter and anterior temporalis muscles. Questionnaires and clinical assessment were used to identify probable sleep bruxers, as reported by Lobbezoo et al. 1 To be included in the study, patients had to be aware of tooth grinding activity and had to fulfill the following criteria in accordance with the American Academy of Sleep Medicine 24 : self-report or report by a bed partner of sound associated with tooth grinding or tooth clenching and one of the following: (1) tooth wear or shiny spots on dental restorations; (2) frequent reports of stiffness, fatigue, or discomfort in the jaw muscles upon awakening; or (3) masseter muscle hypertrophy on voluntary contraction. Exclusion criteria were a history of neurologic or psychiatric disorders; previous diagnosis or signs and symptoms of other sleep disorders (e.g., snoring, sleep apnea, and periodic limb movement); use of prescription medicine or other drugs with possible sleep effects or alterations of motor behavior; smoking, alcohol abuse, and consumption of more than 3 cups of coffee per day; electrode gel allergy; being currently under medical or dental treatment; use of a pacemaker or implanted defibrillator; and some dental characteristics, such as loss of more than 2 posterior teeth except third molars and wearing of removable partial or full dentures. The project was conducted in accordance with Declaration of Helsinki guidelines and was approved by the local ethics committee. Written informed consent was obtained from all participants. A total of 39 individuals were initially evaluated, and 16 were excluded for not meeting the inclusion criteria. Accordingly, 23 subjects were eligible and agreed to start treatment. After 1 week, 6 patients withdrew from the study because of difficulties in wearing the device, and 2 withdrew for missing appointments and records. After that, 15 individuals, 3 men and 12 women, composed the final study sample. Study design This pilot study was designed as a single-blind, randomized clinical trial. On the first day, all participants were asked to complete a Brazilian Portuguese translation of the RDC/TMD questionnaire ( The RDC/TMD clinical examination was performed by 2 calibrated examiners (L.B., J.S.B.). Initially, to record baseline levels of anterior temporalis muscle activity, all participants wore a portable single-channel EMG device (Grind- Care, Medotech A/S) during sleep for at least 5 nights during 1 week (phase 1). At the second visit (day 7 2 days), data were transferred and saved in a personal computer (PC) equipped with commercial software (GrindCare Manager, Medotech A/S). The data analysis provided information about the proper device use by the patient. PI and PPT in jaw muscles were recorded (phase 1). After that, patients were randomly allocated into 2 groups to use the portable EMG device for at least 10

3 OOOO ORIGINAL ARTICLE Volume 117, Number 1 Conti et al. 47 Table I. Session procedure and visit schedule for each patient based on the study design Session procedure/ visit schedule Sample criteria RDC/TMD questionnaire and clinical examination Informed consent Visual analog scale used for pain intensity recording Baseline (day 0) X X X After phase 1 (day 7 2 days) After phase 2 (day 21 2 days) After phase 3 (day 28 2 days) X X X Algometry X X X RDC/TMD, Research Diagnostic Criteria for Temporomandibular Disorders. 23 nights (phase 2): (1) the active group (n ¼ 7; 2 men and 5 women; age, years), in which the device was activated with feedback using the CES paradigm; and (2) the control group (n ¼ 8; 1 man and 7 women; age, years), in which the device did not provide any CES but only recorded EMG activity. The group allocation was done according to a randomized list made with Microsoft Excel software. Patients in the control group were not aware of the inactivity of the device. At the third visit (day 21 2 days), data from GrindCare were again transferred and saved in a PC equipped with commercial software (GrindCare Manager, Medotech A/S). It was thus possible to check whether the patient had used the device correctly. PI and PPT in jaw muscles were also obtained (phase 2). In phase 3 (follow-up), all participants again wore the portable EMG device for more than 5 nights without feedback, to measure jaw muscle activity after intervention. At the fourth visit (day 28 2 days), the patients returned the GrindCare devices, and PI and PPTs of jaw muscles were recorded. Data from GrindCare were again transferred and saved in the PC equipped with commercial software (GrindCare Manager, Medotech A/S). The visit schedule and session procedures are described in Table I. Feedback device and EMG analysis. The device (GrindCare, Medotech A/S) has a single-electrode assembly, with 3 electrode contacts. The electrode was designed to be placed over the anterior temporalis area, which provides the same type of EMG information as obtained from the masseter during sleep. The device analyzed events of EMG activity, according to the signal recognition algorithm described by Jadidi et al. 12 To determine the individual contraction parameters, every night participants were requested to relax their jaw muscles for 10 seconds, then to clench their teeth around 60% of the maximum voluntary contraction for 10 seconds. The determination of the number of events was done based on the algorithm, which considered an event to be when the EMG activity exceeded the previously adjusted signal level at rest plus 20% of the maximum EMG level during the 60% contraction. 12 The feedback circuit based on the CES paradigm was controlled by a microprocessor, where it was possible to adjust and set the intensity of the electrical stimulus. 12 In the active group, in phase 2, patients were able to adjust and set the intensity of the CES to a nonpainful level. The electrical stimulus should be clearly perceived but not uncomfortable or painful. All participants received comprehensive training for the appropriate use of the device. Participants received, on a daily basis, inquiring about the device use and encouraging them to take notes about the data provided by the device. The number of EMG events per hour (EMG/h) was recorded in all nights of each phase. PI. After each phase, the PI during the last week was measured with a 100-mm visual analog scale (VAS). One end of the line was denoted with no pain and the other end with most pain imaginable. Patients were instructed to mark, with a vertical line, the place along the horizontal line where they believed their level of pain was best represented. PPT. PPT was obtained with a digital algometer (Kratos Equipamentos Industriais, Cotia, São Paulo, Brazil) containing a rod with a 1-cm 2 flat, circular tip at one end, which was used to apply the pressure over the muscle. The pressure application was set at approximately 0.5 kgf/cm 2 /s. 18 The body of the masseter and the anterior belly of the temporalis muscles were tested on both sides in a relaxed posture. Each muscle was randomly tested only once by the examiners (J.S.B. or L.B.), who were previously calibrated for muscle locations. PPT was defined as the pressure needed for the participant to report just barely painful, that is, the transition from a nonpainful pressure sensation to the very first painful sensation. Throughout the examination, the individual s head was firmly supported by the operator shand. The device used in the present study had a button that the patient was asked to press at the very beginning of pain sensation. This means that the subject had full control to determine the moment when the applied pressure became painful, with no interference from the examiner. The lowest PPT (on either the left or right side) in the masseter (PPTm) and in the anterior temporalis (PPTat) were considered after each phase for statistical purposes.

4 ORAL MEDICINE OOOO 48 Conti et al. January 2014 Table II. Descriptive data from sample with comparison between groups All samples Active group (n ¼ 7) Control group (n ¼ 8) Differences between groups* Variable Mean SD Mean SD Mean SD P (CI 95%) Age (y) ( 6.5; 17.4) EMG/h ( 22.6; 8.7) PI (mm) ( 2.4; 3.3) PPTat (kgf/cm 2 ) ( 369.9; 484.9) PPTm (kgf/cm 2 ) ( 559.9; 399.9) SD, standard deviation; EMG/h, electromyographic events per hour of sleep; PI, pain intensity; PPT, pressure pain threshold; at, anterior temporalis; m, masseter; CI, confidence interval. *Mann-Whitney test. Statistical analysis The EMG/h, PPT, and PI data were described as mean standard deviation (SD). Baseline (phase 1) data were used to test the correlation between EMG activity and pain parameters for the entire sample with Spearman rank correlation (rho), and Mann-Whitney tests were used to analyze EMG activity and pain variables between groups. A 2-way analysis of variance (ANOVA) was used to test the effect of CES on EMG activity and pain parameters for the entire sample. An ANOVA for repeated measures was used to compare variables intragroup during the 3 phases of the study. Tukey tests were used for post hoc comparison when appropriate. The level of significance was set at 5%. RESULTS Active and control group participants did not differ regarding any characteristic at baseline (Table II). When considering the entire sample at baseline, a moderate positive correlation was found between EMG/h and PPTm (r ¼ 0.614) and between EMG/h and PPTat (r ¼ 0.506) (Figure 1). EMG/h After the first week measuring EMG activity, the mean number of EMG/h for all individuals was The scores for the active group ( ) and the control group ( ) were not significantly different (see Table II). In phase 2, the active group, which received CES, showed a 35% reduction in average EMG/h ( ) compared with the baseline value. In the control group, the average EMG/h was In phase 3, participants in the active group maintained a reduction of average EMG/h when compared with the baseline value ( ). In the control group, the average EMG/h was There was a significant interaction between groups and phases for EMG/h data (F ¼ 5.96; P ¼.003; Figure 2). In phase 2, the mean EMG activity was lower in the active group than in the control group (Tukey test, P ¼.004). In Fig. 1. Scatterplot of mean of electromyographic events per hour of sleep in 5 nights versus mean of pressure pain threshold in masseter muscle at baseline (phase 1). There is a moderate positive correlation (r ¼ 0.614). phase 3, the active group continued to have fewer events per hour than did the control group, although the difference was not significant (Tukey test, P >.05). When analyzing individual groups throughout the experiment (intragroup analysis), significant differences in EMG/h between phases (F ¼ 6.56; P ¼.002; see Figure 2) were found only for the active group, in which lower EMG activity during phase 2 (Tukey test, P <.05) and phase 3 (Tukey test, P <.05) compared with baseline were detected. No difference in EMG activity among phases (F ¼ 2.03; P ¼.136) was encountered for the control group. PPT In phase 1 (baseline), the mean PPT values in the anterior temporalis muscle (PPTat) were and kgf/cm 2, respectively, for the active and control groups. The mean PPT values in the masseter muscle (PPTm) were and kgf/cm 2 for the active and control groups, respectively (P >.05; see Table I). Although the data showed a reduction in EMG/h with CES, there was no significant interaction between groups and phases in PPTat (F ¼ 0.26; P ¼.776) and PPTm (F ¼ 0.22; P ¼.801; Figure 3).

5 OOOO ORIGINAL ARTICLE Volume 117, Number 1 Conti et al. 49 Fig. 2. Bar shows mean of electromyographic events of anterior temporalis muscle per hour of device use (EMG/h) and standard deviation (vertical lines) by period in the study and control groups. There was a significant interaction between groups and phases for EMG/h data (F ¼ 5.96; P ¼.003). *Significant difference between the active and control groups (Tukey test, P ¼.004). **Significant differences in EMG/h between phases (F ¼ 6.56; P ¼.002) in the active group, during phase 2 (Tukey test, P <.05) and phase 3 (Tukey test, P <.05), compared with baseline (phase 1). PI In phase 1 (baseline), the mean PI values were and for the active and control groups, respectively (P >.05; see Table II). Again, although a reduction in EMG/h with CES was detected, no significant interactions between groups and phases were found (F ¼ 0.20; P ¼.823; Figure 4). DISCUSSION The use of CES in the anterior temporalis region was effective in reducing jaw muscle activity during sleep. During the period with active feedback, patients in the active group had 35% lower EMG activity, and this effect remained for 1 week at least, with 38.4% lower EMG activity, when compared with the baseline. This EMG reduction, however, did not influence the selfreported pain or PPT levels. The detected difference between groups after phase 2 could not be attributed only to the CES effect. An increased activity in the controls during phase 2, influenced by time effect, may have contributed to the difference. Nevertheless, the CES activation was capable of reducing anterior temporalis EMG activity values, as can be seen when intragroup analysis is considered. Jadidi et al. reported a reduction of anterior temporalis EMG activity of about 50% after 3 weeks of CES in patients with SB. 12,13 One can hypothesize that if CES had been used in the present study for an extended period, perhaps this reduction might have been even more pronounced. As previously reported, the effect of CES persisted for more than 1 week, even when the CES was Fig. 3. Bar shows mean of pressure pain thresholds (kgf/cm 2 ) in the anterior temporalis (A) and masseter (B) and the standard deviation (vertical lines) by period in the study and control groups. disabled. This could represent the final goal of feedback therapy, which could be considered a learning or conditioning process, yielding a decrease of muscle hyperactivity for long periods. 13 These long-lasting effects, however, were not tested in our study, although a recent study found that the frequency of EMG events could return to baseline levels in follow-up. 16 A note of caution, however, is needed when comparing these studies, because there are significantly different methodologic issues. Some studies used a longer treatment period 13,16 with a crossover design. 13 Although diagnostic criteria and sample size were similar to those of Jadidi et al. 13 and referred to probable SB, the diagnosis of definite SB should be based on self-report, a clinical examination, and a PSG recording, preferably along with audio/video recordings, 1,25 as suggested by Raphael et al. 16 As previously found, 13,16 our results also indicated no effects on self-reported PI. The PI SD values indicate substantial interindividual variation that contributed to the absence of statistical power and an inability to detect changes for this parameter. Moreover, the PI recordings at home were not used, although they might be more accurate. A recent study, however, found that electrical stimulation not only reduced muscle activity but also might

6 ORAL MEDICINE OOOO 50 Conti et al. January 2014 Fig. 4. Bar shows mean of self-reported pain intensity (0-to- 10 visual analog scale) and standard deviation (vertical lines) by period in the study and control groups. be able to decrease PI, restrictions on activities of daily life, and the number of painful muscles on palpation. 15 PPT reflects the pressure that the individual first perceived to be painful. 17 Decreased PPT could reflect an increased excitability at any point of the nociceptive pathway 26 and seemed to be one of the most pronounced differences between patients and asymptomatic controls in a large case-control study in which a variety of mechanical and thermal stimuli were tested. 14 These factors endorse our choice to use PPT in this study. The lowest PPTs were found for the masseter muscle, regardless of the period, which was also the case in a previous study when compared with an asymptomatic population. 18 The exact relationship between jaw muscle activity during sleep and PPT levels is still to be defined. It is nevertheless interesting to note that we found a positive moderate correlation between EMG activity and PPT in masseter muscles at baseline (i.e., the more activity, the higher the PPT), indicating a possible adaptation process instead of a pain-causing factor. 27,28 This finding could explain the absence of relationship between decreased EMG activity, reported pain, and PPT. However, it must be said that the present study design does not allow us to draw any definitive conclusions on the causal relationships between jaw muscle activity and craniofacial pain. Corroborating the pain adaptation model, 28 studies based on PSG recordings found no strong association between bruxism and facial pain and projected an inverse relationship between masticatory muscle activity and PI. 3,5,7,8 Instead, bruxers with lower frequency of motor activity had almost 4 times more chances to report masticatory muscle pain and fatigue, 6 and even SB seemed to be more likely for those reporting less myofascial TMD pain. 3 A recent EMGbased study reported no major differences in EMG activity, recorded with the GrindCare device during sleep, between patients with various craniofacial pain conditions and pain-free individuals. The correlations between EMG events per hour of sleep and the number of painful sites were significant but weak. 29 It could be assumed that psychologic, behavioral, and even genetic variables may play a decisive role in the determination of muscle pain perception, and that such factors may be more important than the simple level of EMG activity or the amount of clenching or grinding during the night. The participation of central neuronal alterations (central sensitization), typical of chronic conditions, can also explain the weak correlation between pain and EMG activity found in the present investigation. 14 Moreover, the effect of muscle hyperactivity could differ according to the patient s condition. Chronic pain patients could have peripheral and central alterations, often related also to impaired endogenous inhibitory control mechanisms. In this condition the patients may be sensitive to afferent stimuli such as muscle hyperactivity. Patients with tension-type headache or migraine could elicit a headache attack after sustained tooth clenching (<30% maximum voluntary contraction). 30,31 Patients with TMDs also have higher levels of catastrophizing complaints, depression or anxiety symptoms, and poor quality of sleep It is suggested that psychologic factors, such as depression and anxiety, could influence the association between pain and motor activity. 33,36 In a small short-term study, however, CES did not influence depression scores. 12 This hypothesis, however, was not tested in our study. After phase 1 of the study, 6 patients experienced difficulties with the device wear and were excluded, reducing our sample size, which is a limitation of the present study. A similar finding was also reported in the study by Bernhardt et al., 15 who found that the operation of the GrindCare device is not easy for all patients. Some problems, such as lost electrodes, that could prevent the feedback or EMG measurement, as well as compliance issues (participants forgot or could not use the EMG device), led us to reduce the number of nights chosen for this study to 5 nights per week. The same problems were reported in a previous study using this device. 29 The lower cost is a great advantage of home recordings. 37 It has been found that patients with painful conditions had higher night-to-night variability of EMG activity when compared with pain-free individuals. 29 So the record of more than 2 nights to verify EMG activity was a positive point of this study. The EMG records with single-channel devices were able to monitor the EMG activity of a single muscle; they were not suitable to gather information on more complex patterns of muscle activity, 4 and they could not differentiate awake periods from sleep periods. 16 Raphael et al. 16 suggested caution when considering

7 OOOO ORIGINAL ARTICLE Volume 117, Number 1 Conti et al. 51 EMG detected with GrindCare, because it has not yet been validated as an accurate tool for SB detection. A good linear fit between the scoring method using singlechannel EMG and the full PSG scoring was found, however. 38 The short-term nature of treatment and evaluation and the relatively small number of individuals are limitations of the present investigation and need to be considered when judging the actual findings. Small differences in mean pain score could become statistically significant with larger samples. But despite the limitations, there was no difference between groups in all initial parameters, and the sample size was sufficient to detect a significant decrease in EMG episodes per hour of sleep after CES. 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