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J Dent Res 85(1):69-73, 2006
© 2006 International and American Associations for Dental Research


RESEARCH REPORT
Biological

Overall Activity of All Masticatory Muscles during Lateral Excursion

S. Yamaguchi1, H. Rikimaru1, K. Yamaguchi2, M. Itoh2, and M. Watanabe1,*

1 Division of Aging and Geriatric Dentistry, Tohoku University Graduate School of Dentistry, 4-1 Seiryo-machi, Aoba-ku, Sendai, 980-8575, Japan; and
2 Division of Nuclear Medicine, Cyclotron and Radioisotope Center, Tohoku University, 2-1 Aoba, Aramaki, Aoba-ku, Sendai, 980-8578, Japan

* corresponding author, makoto-w{at}mail.tains.tohoku.ac.jp


   ABSTRACT
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS & METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Quantification of the overall activity of every masticatory muscle is requisite for the analysis of stomatognathic function, which has not been accomplished by conventional electromyography. We used positron emission tomography and 18F-fluoro-deoxy-glucose to quantify the overall activity of every masticatory muscle during lateral excursion, and to evaluate the relative contribution of each masticatory muscle to lateral excursion. The present study suggested that lateral and medial pterygoid muscles are more responsible for lateral excursion than are masseter and temporal muscles. In particular, the contralateral lateral pterygoid muscle plays a major role, followed by the contralateral medial pterygoid muscle.

KEY WORDS: positron emission tomography • 18F-fluoro-D-deoxyglucose • lateral excursion • masticatory muscle


   INTRODUCTION
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS & METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Quantification of masticatory muscle activity is necessary for analysis of stomatognathic function. Electromyography has been utilized to record the activity of masticatory muscles, and masseter and temporal muscles have been frequently analyzed by electromyography (Blanksma and Van Eijden, 1990; Blanksma et al., 1992), since these muscles are easily accessible from the skin surface. In contrast, less information is available about the activity of other masticatory muscles, i.e., medial and lateral pterygoid muscles (Hannam and McMillan, 1994), since surface electromyography cannot be applied, and the alternative approach to electromyographic recording, the use of a wire or needle electrode, is difficult to perform: The anatomical locations of these muscles are deep below the skin surface, and determining the electrode location is difficult. Furthermore, intramuscular electromyographic recording evaluates the activity only in a limited region of a muscle, but cannot quantify its overall activity.

Recently, positron emission tomography and 18F-fluoro-deoxy-glucose (FDG-PET) have been used to evaluate muscle activity by measuring intramuscular variation in glucose metabolism within exercising skeletal muscles (Fujimoto et al., 1996; Tashiro et al., 1999; Pappas et al., 2001; Oi et al., 2003). A previous study has shown that the FDG-PET can simultaneously quantify the overall activity of individual masticatory muscles during chewing, and without any physical invasion (Rikimaru et al., 2001, 2002), which is not achievable with conventional electromyography.

The present study was designed to quantify the overall activity of lateral and medial pterygoid muscles and masseter and temporal muscles by FDG-PET, and to compare their contributions to the lateral jaw movement, in which the lateral pterygoid muscle has been shown to play an important role (Murray et al., 2001).


   MATERIALS & METHODS
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS & METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Subjects
Eleven healthy young male volunteers participated in the study. The volunteers were 24-31 yrs old (mean age, 27.0 ± 1.5 yrs) and had normal masticatory function. Their plasma glucose concentration was within the normal range (78-108 mg/dL) at the time of the study. Prior to PET evaluation, written informed consent was obtained from each subject after a full explanation of the study was provided. This study was approved by the Clinical Committee for Radioisotope Use of Tohoku University and the Ethical Committee of Tohoku University Graduate School of Dentistry.

PET Imaging
Subjects were instructed to avoid eating and drinking for at least 4 hrs before the start of the experiment. Each subject received an injection of 39.2 ± 5.2 MBq of 18F-FDG into the cubital vein, following a quiet 10-minute sitting period. Just after the injection, each subject was asked to start repetition of leftward jaw motion to the canine edge-to-edge position, and rightward jaw motion back to the midline, at a frequency of 1.0 Hz (paced by a metronome) and without exerting a biting force. This continued for 30 min while the subject was in a sitting position, monitored by an examiner. All subjects were asked to practice the repetitive jaw movement before the 30-minute exercise period. A period of 30 min was required for sufficient accumulation of FDG in masticatory muscles to allow for analysis of the PET images. The PET images were acquired after completion of the exercise.

PET scanning was performed by a SET-2400W three-dimensional PET scanner (Shimadzu Co., Kyoto, Japan) with a full-width half-maximum spatial resolution of 7.9 mm (axial) and 3.9 mm (trans-axial) at the center of the 20.0-cm axial field of view (Fujiwara et al., 1997). Thirty-five min after injection of 18F-FDG, head and neck images were acquired for 15 min, while the subject was in a supine position. Tissue attenuation of annihilation gamma rays was corrected by post-injection transmission scans in a rotating 68Ge/68Ga source. Acquired three-dimensional raw data were reconstructed into 94 slices by means of an ‘ordered subsets expectation maximization’ algorithm on a XP-1000 workstation (Digital Equipment Corporation, Boston, MA, USA) (Hudson and Larkin, 1994).

MRI imaging
T1-weighted magnetic resonance images (MRI) of the head and neck of each subject were obtained with a spoiled gradient echo sequence after the PET study. The equipment used was a SIGNA MR/i 1.5T (General Electric Medical Systems, Waukesha, WI, USA).

Image Analysis
Image processing and regions-of-interest analysis were carried out with PET-MRI Tools (Varga, 2000) integrated with the "Automated Image Registration" algorithm (Woods et al., 1993) on Matlab (Math Works, Natick, MA, USA). We re-aligned MR images to corresponding PET images using the "Automated Image Registration" method to determine the location and structure of the masticatory muscles in the PET images. This PET-MRI registration method has most commonly been used in brain PET studies, since it can add anatomical information to functional PET images by alignment of a corresponding MR image with the objective PET image. Regions-of-interest were manually drawn over every masticatory muscle on all slices of registered MR images, and these were applied to the corresponding PET images (Fig. 1Go). The mean value of the radioactivity per voxel in each region-of-interest was automatically measured with PET-MRI Tools and normalized for both the amount injected and the subject’s body weight, to give a standardized uptake ratio as an indicator of muscle activity, according to the following formula (Kubota et al., 1985; Strauss and Conti, 1991; Schomburg et al., 1996):



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Figure 1. Regions-of-interest over each masticatory muscle. Registered MR (left) and PET (right) images at the same slice level in the same subject. Black-white and color scales depict the MR signal intensity and the accumulation of FDG, respectively. Regions-of-interest are color-coded as follows: pink and yellow = right and left masseter muscles, purple and blue = right and left temporal muscles, green and orange = right and left medial pterygoid muscles, white and red = right and left lateral pterygoid muscles.

 

The standardized uptake ratio is a relative semi-quantitative value of radioactivity in regions-of-interest, which can be understood as the concentration of radiotracer in the region-of-interest divided by the concentration of injected dose distributed throughout the mass of the body. The standardized uptake ratio for each masticatory muscle is expressed as a mean ± standard deviation.

Statistical Analysis
The statistical significance of differences among all masticatory muscles was examined with a one-factor analysis of variance and the Games/Howell method. In addition, a comparison between the contralateral and ipsilateral activities of each muscle was performed with a Student’s t test. A p value of less than 0.05 was considered to be significant.


   RESULTS
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS & METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Standardized Uptake Ratio of All Masticatory Muscles in Each Subject
The standardized uptake ratio of the contralateral lateral pterygoid muscle was the largest among all masticatory muscles in eight out of the 11 subjects (TableGo) (B, C, D, E, G, H, I, K), and the standardized uptake ratio of the contralateral medial pterygoid muscle was the second largest among all masticatory muscles in seven subjects (A, B, C, D, E, H, K). The standardized uptake ratios of the contralateral lateral and medial pterygoid muscles were higher than those of the bilateral masseter and temporal muscles in all subjects, and the standardized uptake ratios of all pterygoid muscles were higher than those of all bilateral masseter and temporal muscles in nine subjects (A, B, C, E, F, G, I, J, K).


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Table. Standardized Uptake Ratios Indicating 18F-fluoro-D-deoxyglucose Uptake per Unit Volume of Masticatory Muscle Induced by Lateral Excursion
 
Mean Standardized Uptake Ratio of the Masticatory Muscles
The mean standardized uptake ratios of all 4 pterygoid muscles were higher than those of the bilateral masseter and temporal muscles (Fig. 2AGo). Statistical analysis revealed significantly higher mean standardized uptake ratios (p < 0.05 by the Games/Howell method) in the contralateral lateral and medial pterygoid muscles, compared with the bilateral masseter muscles.



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Figure 2. The mean and standard deviation of the standardized uptake ratios in masticatory muscles for 11 subjects. (A) Comparison of the standardized uptake ratio among all masticatory muscles. Statistical significance was tested by a one-factor analysis of variance and the Games/Howell method (*p < 0.05). (B) Comparison of the standardized uptake ratio between the contralateral and ipsilateral muscles. Statistical significance was examined with Student’s t test (*p < 0.05). R = Right (Contralateral side); L = Left (Ipsilateral side); SUR = Standardized uptake ratio.

 
A comparison between the contralateral and ipsilateral mean standardized uptake ratios of each masticatory muscle showed that the mean standardized uptake ratio of the contralateral lateral pterygoid muscle was significantly higher than that of its ipsilateral counterpart (p < 0.05 by Student’s t test) (Fig. 2BGo). The mean standardized uptake ratio of the contralateral medial pterygoid muscle was also higher than that of its ipsilateral counterpart, but the values were not significantly different. There was little difference between the mean standardized uptake ratios of the ipsilateral and contralateral masseter and temporal muscles.

FDG Accumulation in PET-MRI Fusion Images
The contralateral lateral pterygoid muscle of subject C showed the highest standardized uptake ratio of all the subjects (TableGo). In this subject, obvious accumulation of FDG was observed in the contralateral lateral and medial pterygoid muscles, the brain, and the sublingual gland, but was not clearly detected in the bilateral masseter and temporal muscles (Fig. 3Go). FDG accumulation in the brain and the sublingual gland was observed in all subjects.



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Figure 3. PET-MRI fusion images of the head and neck, induced by left lateral excursion. Left upper and lower images are frontal and sagittal images in one subject (subject C: see TableGo). Red lines (A-F) show the levels of transverse scans shown in the center and right images. TM = temporal muscles, LP = lateral pterygoid muscles, MP = medial pterygoid muscles, MM = masseter muscles, SLG = sublingual glands.

 

   DISCUSSION
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS & METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
FDG-PET
An FDG-PET image is a three-dimensional map of FDG distribution that reflects glucose metabolism in the body. Hence, the physiological activity of body tissues, including masticatory muscles, can be visually evaluated from FDG accumulation in PET images. Previous reports have confirmed that FDG accumulation was correlated with muscle activity in a rabbit experimental model (Mossberg et al., 1989, 1993). Fig. 3Go presents a typical example of such an image, showing FDG accumulation in the contralateral lateral and medial pterygoid muscles during lateral excursion. FDG accumulation in these muscles indicates that they have high activity during lateral excursion, since FDG has previously been reported to be accumulated in the brain and sublingual gland, but not in any masticatory muscles under resting conditions (Jabour et al., 1993). In the present study, we propose that FDG-PET can be applied to quantify the overall activity of every masticatory muscle during lateral excursion.

PET-MRI Registration
We applied, for the first time, the "Automated Image Registration" method (Woods et al., 1993) to the analysis of skeletal muscles, based on the assumption that the relative physical relationship between the brain and each masticatory muscle is unchanged when the mandible is held in an occlusal position. The "Automated Image Registration" algorithm is an established program that allows for accurate automated registration of three-dimensional images of the brain mathematically across various imaging modalities. It was difficult to define regions-of-interest tracing the anatomical outline of the masseter, temporal, and ipsilateral lateral and medial pterygoid muscles using PET images only, because of low FDG accumulation in these muscles. To overcome this problem, we applied the PET-MRI registration method and defined accurate regions-of-interest over each masticatory muscle on the anatomical MR images registered to the corresponding PET images (Fig. 1Go). Hence, the PET-MRI registration method is beneficial for quantification of the overall activity of all masticatory muscles.

Overall Activity of Each Masticatory Muscle
FDG-PET facilitates analysis of the activity of each masticatory muscle during various jaw movements within a certain period of time, based on quantitation of glucose metabolism, whereas conventional electro-myography examines instantaneous muscle activity based on electrical signals from the muscles. The present results show that the activities of the pterygoid muscles, and particularly the contralateral pterygoid muscles, are higher than those of the masseter and temporal muscles during lateral excursion.

Lateral and Medial Pterygoid Muscles
Analysis of the quantitative data for glucose metabolism corresponding to muscle activity confirms the results of previous electromyographic studies that have indicated that the lateral and medial pterygoid muscles are involved in horizontal jaw movements (Hannam and Wood, 1981; Gibbs et al., 1984; Widmalm et al., 1987; Murray et al., 2001, 2004), further suggesting that the contralateral lateral pterygoid muscle plays the most important role during lateral excursion, and that the contralateral medial pterygoid muscle is of secondary importance. Previous studies have showed that intercuspal clenching initiates greater activity of the medial pterygoid muscles when the bite force is directed anteriorly, compared with vertical intercuspal clenching (Wood, 1986), which suggests that the medial pterygoid muscles pull the mandible forward. The present study suggests that the high activity of the contralateral medial pterygoid muscle represents the generation of a forward force to pull on the contralateral angle of the mandible during lateral excursion.

Masseter and Temporal Muscles
The activity of the masseter and temporal muscles were lower compared with those of the pterygoid muscles, and there was little difference between the ipsilateral and contralateral activity of these muscles. These results do not concur with previous electromyographic reports of the activities of the ipsilateral temporal muscle and the contralateral masseter muscle during lateral excursion (Vitti and Basmajian, 1977; Gibbs et al., 1984). The present results were obtained by quantification of the overall masticatory activity in multiple paths of leftward jaw motion with rightward motion to the midline over a 30-minute period, whereas the previous electromyographic studies may have recorded instantaneous partial activity of the masseter and temporal muscles in a single path of jaw motion. Therefore, the conditions used in the present study resulted in little difference between the ipsilateral and contralateral activities of the masseter and temporal muscles. Comparison of the overall masticatory activity suggests that the contributions of the masseter and temporal muscles to lateral excursions without bite force are small, compared with those of the pterygoid muscles.

Prospects
The present study shows that the use of FDG-PET allows for quantification of the overall activity of every masticatory muscle and the evaluation of the relative contribution of each masticatory muscle to any particular jaw movement. A time-based measurement of motor unit activities by FDG-PET is impossible because of its lower time and spatial resolutions, compared with electromyography. However, FDG-PET allows for comparison of the total workload in various muscles during a certain period of time on a common scale, which indicates glucose metabolism per unit volume, and therefore this method has potential clinical application in the diagnosis of muscle disorders caused by large loading. Development of novel PET-tracers may provide a new perspective for the analysis of muscle activity and for clinical applications.


   ACKNOWLEDGMENTS
 
We thank Seiichi Watanuki and Masayasu Miyake for creating the PET images, and Dr. Hiroshi Shamoto for conversion of the MR images. Gratitude is expressed to the staff at the Division of Aging and Geriatric Dentistry, Tohoku University Graduate School of Dentistry, for their support, and to the entire staff at the Cyclotron and Radioisotope Center, Tohoku University, for their collaboration. This study was supported by Grants-in-Aid (Nos. 13470408 and 13877324 to M. Watanabe) for Scientific Research from the Japan Society for the Promotion of Science.

Received October 19, 2004; Last revision September 2, 2005; Accepted September 29, 2005


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 DISCUSSION
 REFERENCES
 
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This Article
Right arrow Abstract Freely available
Right arrow Figures Only
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Right arrow Similar articles in ISI Web of Science
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Right arrow Download to citation manager
Citing Articles
Right arrow Citing Articles via ISI Web of Science (3)
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Right arrow Articles by Yamaguchi, S.
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Right arrow Articles by Yamaguchi, S.
Right arrow Articles by Watanabe, M.


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