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Antero-posterior activity changes in the superficial masseter muscle after exposure to experimental pain ARTICLE in EUROPEAN JOURNAL OF ORAL SCIENCES · MAY 2002 Impact Factor: 1.49 · DOI: 10.1034/j.1600-0722.2002.11198.x · Source: PubMed
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Eur J Oral Sci 2002; 110: 83–91 Printed in UK. All rights reserved
Copyright # Eur J Oral Sci 2002
European Journal of Oral Sciences ISSN 0909-8836
Antero-posterior activity changes in the superficial masseter muscle after exposure to experimental pain
Jens C. Tu¨rp1, Hans J. Schindler2, Maria Pritsch3, Qiguo Rong4 1
Department of Prosthodontics, Dental School, University of Freiburg, Germany, 2Federal Research Center for Nutrition, Karlsruhe, Germany, 3Department of Medical Biometry, University of Heidelberg, Germany, 4Institute of Mechanics, University of Karlsruhe, Germany
Tu¨rp JC, Schindler HJ, Pritsch M, Rong Q. Antero-posterior activity changes in the superficial masseter muscle after exposure to experimental pain. Eur J Oral Sci 2002; 110: 83–91. # Eur J Oral Sci, 2002 The aim of this randomized, controlled, double-blind study was to examine how the activation pattern of the masseter muscle changes during natural function when experimental pain is induced in a discrete anterior area of the muscle. In 20 subjects, three bipolar surface electrodes and three intramuscular fine-wire electrodes (antero-posterior mapping) were simultaneously attached above and in the right masseter muscle to record the electromyographic (EMG) activity during unilateral chewing before and after infusion of a 0.9% isotonic and 5% hypertonic saline bolus in the anterior area of the muscle. The activity of the contralateral masseter muscle was registered by surface electrodes. In addition, the development of pain intensity was quantitatively measured with a numerical rating scale (NRS). While both saline concentrations caused pain, the hypertonic solution evoked stronger pain. The experiments also provided evidence of a significant although differential activity reduction of the ipsilateral masseter muscle in the anteroposterior direction. The activity reduction decreased with increasing distance from the location of the infusion. The results support the idea that the strategy of differential activation protects the injured muscle while simultaneously maintaining optimal function.
Pain elicited by infusion of hypertonic saline has proven to be a suitable model to simulate clinical muscle pain (1–3). In experimental pain studies, the individual jaw muscle is usually viewed as a homogeneous unit; the results from experiments are correspondingly interpreted as applying to the muscle as a whole (3, 4). This concurs with the traditional concept that all motoneurons of a specific muscle receive the same synaptic input (5) and that they are activated in a predetermined order corresponding to their cell size (6). More recent findings (7–12) let us assume, however, that the complexly composed masseter muscle, similar to the complex limb muscles (13–15), shows a deviation from such homogeneous activation. In other words, there is evidence that the various areas of the muscle are capable of differential or heterogeneous activity. In contrast to the ‘mosaic pattern’ in the extremities with fiber distribution throughout large areas of the muscle cross-section (16), the more focal distribution of the motor units in the jaw muscles (17), as well as the regional heterogeneous, histochemical fiber profile (18), point to local functional differences. The regional differences in the jaw muscle activation might make painful microlesions, single motor unit fatigue, or both, caused by, for example, repetitive strain (19–23), more plausible than in the case of a homogeneously structured muscle with the same synaptic input, because a differential motor
Jens C. Tu¨rp, Department of Prosthodontics, Dental School, Albert Ludwigs University, Hugstetter Str. 55, 79106 Freiburg, Germany Telefax: +49–761–270925 E-mail:
[email protected] Key words: mastication; myofascial pain; nociception; electromyography; EMG mapping Accepted for publication December 2001
control might favor the development of large regional force vectors (stress concentrations) within the individual muscle. Recent studies confirm focal lesions in the masseter of rats caused by overload (24). However, a necessary prerequisite for such local (potentially overloading) stresses appears to be that the differential activation is maintained even under pain conditions. This is indicated by fatigue studies of jaw muscles, which show that pain is perceived before the beginning of muscle fatigue (21). Unilateral experimental pain studies (electromyographic recorded by a single surface electrode) have shown that saline-induced pain causes decrease in EMG activity in the ipsilateral muscle region during the agonistic activity phase (25, 26). No effects were detected on the contralateral side during mastication on the ipsilateral side or during the antagonistic phase (25). To date, no data exists about the synchronous sensorymotor reaction in different muscle regions of a complex muscle under these experimental conditions. Therefore, the main aim of this study was to investigate if, triggered by discrete experimental pain, a differential sensorymotor reaction in the homolateral masseter muscle can be detected. In addition, we evaluated if and how the EMG activity of the contralateral side changes and if the registered EMG activity depends on the registration method (surface vs. intramuscular EMG).
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Material and methods Subjects
Twenty healthy individuals (10 males, average age 27.2 yr, SDt3.4; 10 females, average age 25.3 yr; SDt1.8) participated in the study. All subjects were Caucasians and free of temporomandibular disorders. The study was approved by the Ethics Committee of both the Dental Board of Baden-Wu¨rttemberg and the University of Freiburg Medical School. Informed consent was obtained from all participants. The study was conducted in accordance with the Declaration of Helsinki. Assessment of the experimental muscle pain
In the test sessions, the individual pain perception was determined for all 20 subjects using an 11-digit numerical rating scale (NRS), with 0 representing no pain and 10 representing the greatest pain imaginable. After a 5% hypertonic or 0.9% isotonic saline injection, the current pain was rated by the subject in intervals of 15 s. The subjects indicated their perceived pain by pointing to whole numbers between 0 and 10 on a previously prepared NRS (30 cm long) that was placed level to the chest. When the subjects no longer perceived pain, the rating was stopped. After the experiments, the subjects were requested to describe the quality of pain using an adjective list (27). They also indicated the location, radiation, and referral pattern on a pain drawing of the head and neck. EMG-recordings
EMG recordings were obtained simultaneously (anteroposterior EMG mapping) by surface and intramuscular electrodes. Three bipolar surface electrodes (surface electromyography, SEMG) were attached on the ipsilateral and contralateral side, respectively. The anterior and posterior borders of the masseter muscle were identified by palpation at maximum voluntary contraction and marked. The individualized disposable bipolar surface Ag/AgCl electrodes (conducting surface diameter: 14 mm; Duotrodes, Myotronics, Seattle, WA) were perforated (perforation: 1 mm in diameter) in the middle region of the bipolar electrodes. The anterior electrode received two perforations, separated by 4 mm in a vertical direction. The perforations allowed the insertion of the fine-wires as well as the injection of the saline solution with the surface electrodes in place. The surface electrodes were mounted parallel in a craniocaudal and an antero-posterior direction to the anterior border of the masseter. Additionally, they were aligned to the middle of the distance between the lower border of the zygomatic arch and the lower border of the mandible (Fig. 1). Before placement of the electrodes, the skin was carefully cleaned with 70% alcohol. Additionally, three bipolar fine-wire electrodes were inserted in the ipsilateral masseter muscle (intramuscular electromyography, IEMG). Each electrode consisted of two Teflon-insulated stainless-steel wires (diameter 0.08 mm) with bared tips (2 mm), bent into a hook (California Fine Wire Co., Grover Beach, CA). The distance between the two bare ends was about 2 mm. The electrodes were inserted by means of a 0.4r25 mm disposable hypodermic needle, 15 mm deep in the superficial part of the masseter. The standardized depth was obtained by use of an insertion stop. To avoid an additional session for the test persons, available magnetic resonance images (MRI) of 20 patients (f=10;
Fig. 1. Surface electrodes and intramuscular electrodes placed on the skin and in the right masseter muscle of one subject.
average age 36.0 yr, SDt13.5; m=10; average age 37.7 yr, SDt11.9) were evaluated to determine the adequate penetration depth (depth of the overlying tissue in the prospective penetration areas of the needles: males 9.5 mm, SDt1.1; females 8.9 mm, SDt1.4). The results showed that insertion at a depth of 15 mm reaches the superficial part of the masseter muscle with certainty. The posterior electrodes were placed in a 10u anterior direction, the anterior electrodes in a 10u posterior direction. The intermediate electrodes were inserted perpendicularly. This procedure guaranteed a mean interelectrode distance of about 15 mm. The wire electrodes were secured by tape on the surface electrodes. (Three posterior electrodes had to be replaced because they caused pain during movement.) The ground electrode was positioned on the neck above the seventh vertebra. The EMG signals were amplified differentially (1000r, MP 100 Biopac Systems, Santa Barbara, CA), recorded at 1800 Hz sampling rate, bandpass-filtered (1–500 Hz), and saved. Saline injection
All subjects received 5% hypertonic and 0.9% isotonic saline in a randomized controlled double-blind manner with a two-block cross-over design separated by 1 wk. The solution was injected into the anterior part of the masseter with an 0.33r13 mm insulin needle. The solution was allowed to become room temperature before injection. The complete length of the needle was inserted at light contraction of the masseter through the upper perforation of the anterior surface electrode in a 15u cranial and slightly posterior direction. The cranial direction of the needle and the distance between the two perforations in the surface electrode (4 mm) guaranteed about 8 mm distance between the wire electrode and the needle tip. Afterwards, the subject was instructed to relax the muscle. Thereafter, 0.2 ml of the hypertonic or isotonic saline solution was injected over a time period of 15 s. Test food
Fresh carrots were selected as test food. They were cut into identical sizes measuring 15r10r10 mm using a cutting device. The test food was prepared the day before the experiments and kept in a refrigerator at a temperature of 12uC until starting the experiments. Earlier studies with 17 various types of food (28) showed that chewing this food
Masseter muscle activity in experimental pain texture resulted in almost constant electrical muscle activity and constant force development throughout approximately 10 chewing strokes.
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instead of single chewing burst measurements in the analysis was justified, as the evaluation of the activity reduction in a pilot study (41) revealed no time effect during the course of chewing bursts.
Experimental protocol
Before electrode placement, all subjects were asked if they preferred chewing on the right or left side. Because all test persons reported right side or bilateral chewing, the right masseter was chosen for the experiments. During the experiments, the test subjects sat upright on a chair in a quiet room. For the chewing tests, the test food was placed with a pair of dental tweezers in the subjects’ mouths between the first right molars. The subjects were then instructed to wait for a signal to begin mincing the texture on one side only, to cease chewing upon the second signal (after approximately 11–15 chewing strokes) and then to spit out the remaining minced food. The next piece of carrot was introduced between the teeth in the same way. After one or two test runs, the chewing process, conditioned by now, was recorded three times with surface electrodes only. Afterwards, the fine-wire electrodes were placed, and chewing was recorded again. Following three additional baseline recordings, 5% hypertonic or 0.9% isotonic saline was infiltrated into the anterior part of the masseter muscles using the method described above. The test series were repeated in the same way as the baseline recordings. During the test conditions, the subjects rated pain intensity every 15 s in the above described manner. Each experimental session lasted approximately 50 min. Data analysis
The raw data were exported from the Biopac software (AQUIRE 3.53) and imported into a special mathematical software (MATLAB 3.5) for analysis. The data were rectified with the root mean square algorithm (RMS). The activity bursts registered during chewing were automatically separated into agonist and antagonist phases using a program especially developed for this purpose. The algorithm consists of the following steps: (a) superposition of the three SEMG channels on the chewing side by a normalizing algorithm to form a single signal line, (b) filtering of the resulting data with a higher-order polynome, and (c) specification of the individual, minimal thresholds for the beginning and the end of the EMG bursts. The thresholds were first determined as a quotient of the global mean of all chewing bursts, and subsequently visually confirmed. The raw data were automatically evaluated by the time intervals determined in this way. This procedure was validated with the K6I-system (Myotronics), which permits synchronous recording of EMG and kinematic data during jaw movement (28). By doing so, it could be shown that – after treating the raw data with the algorithm explained above – the beginning of the opening and closing phases agreed very well with the minimal threshold for the beginning and the end of the EMG bursts. The deviation from the exact kinematic turning point in relation to the complete opening or closing phase amounted less than 1% in the mean. In the present study, despite the lack of kinematic data, this procedure provided a good method for the differentiation of agonistic and antagonistic activity phases. The mean RMS values of each subject were determined through 11 chewing strokes and three repetitions. Due to the partially automatic evaluation of the raw data, a person who did not participate in the clinical part of the study was able to carry out the analysis. Evaluation of mean RMS values
Statistical analysis
The influence of the different saline solutions on muscle activity was investigated by the relative differences between baseline measures (baseline 1=EMG recording prior to 5% hypertonic saline injection; baseline 2=EMG recording prior to 0.9% hypotonic saline injection) and by the value after the infusion of the solutions [(baselinextest condition)/ baseliner100], in the following denoted as relative activity reduction (%). We used relative differences, because the two-block cross-over design requires the normalization of the measurements for the respective baseline values. This is the reason why the saline solution factor was included in the variance analysis with only two levels. To investigate the effects before (baseline 3) and after insertion of the wire electrodes, the absolute values of the rectified data were used. The distribution of the measured parameters under the various conditions (baseline measures, isotonic and hypertonic saline, effect of the intramuscular electrodes) and in the various regions of the masseter muscle were described by the mean values and standard deviations. A phase or interaction effect of the relative activity change between isotonic and hypertonic saline was excluded by paired t-test. In order to assess the influence of hypertonic saline in contrast to the isotonic solution or to the influence of the masseter region, a two-way analysis of variance for repeated measures in both factors was performed. The relative activity reduction within the same muscle regions under the test conditions was compared by two-tailed paired t-tests. Following this, various paired comparisons of the individual parameters, detailed in the results section, were made with the two-tailed paired t-test. Only the results of the measurements (surface and wire electrode recordings) taken from the ipsilateral masseter muscle were laid down as confirmatory evaluations. The a-level of the individual tests in the variance analysis and those of the subsequent paired comparisons were adjusted using the Bonferroni-Holm method. The value a=0.05 was assumed as the global significance level. All other evaluations should be interpreted as exploratory and, correspondingly, the specified P-values should be understood as descriptive measures. The statistical analyzes were performed by the statistic software SAS (SAS Institute, Cary, NC, USA), v. 8 for Windows.
Results SEMG – agonistic phase
Ipsilateral EMG-recordings – The investigation of the effects of 5% saline solution on the activity of the masseter muscle during chewing showed a significant decrease in EMG activity in all recorded muscle regions (Fig. 2A). Figs. 3A and B show the raw data of the anterior region of a test person before and after the infusion of 5% hypertonic saline solution. Fig. 4 demonstrates the relatively uniform activity during 33 consecutive masticatory cycles before and after the hypertonic saline infusion. The relative activity
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Fig. 2. Mean RMS amplitudes (mV) of the agonistic activity of the ipsilateral and contralateral masseter muscle in the various muscle regions after infusion of (A) 0.9% isotonic saline and (B) 5% hypertonic saline in comparison to baseline recordings. (C) Relative activity reduction (%) caused by the isotonic and hypertonic solution relative to the baseline recordings (mean value and SD); a=anterior; m=intermediate; p=posterior. IEMG=intramuscular electromyography, SEMG=surface electromyography. Baseline 1=EMG recording prior to 5% hypertonic saline injection; baseline 2=EMG recording prior to 0.9% hypotonic saline injection. Asterisks indicates significant differences (A and B) between the test conditions and (C) the muscle regions (paired comparisons with Bonferroni-Holm adjustment, global significance level a=0.05). mV 3.0
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Fig. 3. Raw data (anterior muscle region) of three masticatory cycles of a test person (A) before and (B) after infusion of 5% hypertonic saline. Upper trace: surface electrodes (SEMG); lower trace: intramuscular electrodes (IEMG). A significant activity reduction of the anterior area in (B) can be clearly recognized in both traces. Notice the different scales for the electric activity.
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Fig. 4. Course of the individual chewing strokes (1–33) in the ipsilateral masseter muscle in the anterior, intermediate, and posterior muscle regions before and after infusion of 5% hypertonic saline (RMS amplitudes [mV], mean value, and SD). The dips at masticatory cycles 1, 12, and 23 each represent the first cycle of the repetitions.
Masseter muscle activity in experimental pain reductions (based on the value without saline infusion) amounted on average to 17.0t12.4% (P
