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Volume Changes in Human Masticatory Muscles between Jaw Closing and Opening
T.K. Goto1,*,
K. Tokumori1,
Y. Nakamura2,
M. Yahagi3,
K. Yuasa1,
K. Okamura1 and
S. Kanda1
1 Department of Oral and Maxillofacial Radiology, Faculty of Dental Science, Kyushu University, 3-1-1, Maidashi, Higashi-ku, Fukuoka, 812-8582, Japan;
2 Department of Radiology, Kyushu University Hospital, Fukuoka, Japan; and
3 Asahi Kasei Joho System Co., Ltd., Tokyo, Japan;
Correspondence: *corresponding author, goto{at}rad.dent.kyushu-u.ac.jp
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ABSTRACT
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Most jaw muscles are complex, multipennate with multiple components. The morphologic heterogeneity of masticatory muscles reflects their functions. We hypothesized that the volume of masticatory muscles changes between jaw closing and opening, and that there is a difference in the volume change among the muscles. Magnetic resonance images of the entire head were obtained in ten normal young adult subjects before and after maximum jaw opening. The volume changes of the masseter, medial, and lateral pterygoid muscles were measured. Only slight changes were seen in the masseter and medial pterygoid muscles. The lateral pterygoid muscle, however, significantly decreased its volume during jaw opening. The results provide normative values of muscle volume in living subjects, and suggest that the volume changes differ among jaw muscles.
Key Words: human masticatory muscles • muscle volume • magnetic resonance imaging • jaw opening
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INTRODUCTION
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The anatomic heterogeneity of masticatory muscles reflects their functions. Histochemical muscle-fiber variations (Eriksson et al., 1981; Eriksson and Thornell, 1983) and anatomical architectural characteristics in cadavers (van Eijden and Raadsheer, 1992; van Eijden et al., 1995, 1997) and in animals (Herring et al., 1984; Miller and Farias, 1988; Langenbach and Weijs, 1990) have been investigated. The heterogeneity of each masticatory muscle in humans—in terms of cross-sectional areas, bite force, relationships with the craniofacial morphology (Gionhaku and Lowe, 1989; Hannam and Wood, 1989; van Spronsen et al., 1989, 1997; Xu et al., 1994; Raadsheer et al., 1999), and muscle lines of action (Koolstra et al., 1990)—has been described. Most investigations have concentrated on the jaw-closing position. We further investigated the relationship between jaw movement and muscle morphology. The variations and movements of jaw-muscle insertions (Goto et al., 1995) and length changes (Goto et al., 2001) were shown by direct measurements of muscle and jaw movements. The volume of muscle is one architectural parameter (van Eijden et al., 1997) including its length and thickness. The length and cross-sectional areas of muscle reflect the force-producing properties; however, the exact changes in muscle volume and the way it changes during jaw movements remain unclear. The changes in the length and thickness of the muscles may compensate for each other. The volume change has been shown to be a function of the length of the muscle and of the amount of tension developed at a given length (Baskin and Paolini, 1967). As far as length and insertion areas showed heterogeneities, we hypothesized that the volume of the masticatory muscles changes after jaw opening, and in addition, there is a difference in the volume change among the muscles.
The purposes of this study were to: (1) determine the normative values of the muscle volume in normal subjects, (2) determine how the volume of the masticatory muscles changes after jaw opening, (3) and investigate the differences among the muscles in volume changes. To test our hypotheses, we designed this investigation to be a non-invasive study using high-quality three-dimensional (3D) reconstructed images from magnetic resonance imaging (MRI).
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MATERIALS & METHODS
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Subjects
The study was carried out in ten normal adults, five females and five males, 20-30 yrs of age. In total, 60 muscles on both the left and right sides of the masseter, medial, and lateral pterygoid muscles were analyzed.
All subjects had normal skull shape, normal occlusion, well-arranged dentitions, and no signs of craniofacial anomalies or temporomandibular disorder. Informed consent, which was reviewed and approved by the Ethics Committee of the Faculty of Dentistry, Kyushu University, was obtained from each of the subjects before the study.
Image Data Acquisition
The subjects underwent an MRI study by means of a 1.5 Tesla (Magnetom Vision, Siemens AG, Erlangen, Germany) with a head coil. Two sets of images were obtained. The subjects clenched teeth slightly in the intercuspal position at jaw closing. At maximum jaw opening, the subjects first opened their mouths as far as possible. Then, they slightly decreased the degree of mouth opening to avoid discomfort while maintaining a maximum opening. Acrylic plastic blocks were set in their mouths during the acquisition of the images. This method for maximum mouth opening is generally used when doctors perform MRI for a diagnosis of temporomandibular disorders.
The high-quality 3D image sets were obtained by means of three-dimensional magnetization-prepared rapid gradient-echo imaging (3D MP RAGE) (Fig. 1 ).
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Figure 1. The high-quality 3D image sets of the entire head (A–C) and phantoms (D) obtained by means of 3D MP RAGE (TR 9.7 ms, TE 4.0 ms, TI 300 ms). The field of view was 230 x 230 mm. (A) Coronal view. LP, lateral pterygoid muscle; MP, medial pterygoid muscle; MS, masseter muscle. (B) Sagittal view. (C) Axial view. The voxels are 0.45 x 0.45 x 1.25 mm. They are displayed as a series of contiguous images at intervals of 1.25 mm. When the contour of difficult parts is traced on the original coronal images, the different sets of contiguous axial, sagittal, or other images are reconstructed and used to confirm the correct position of the muscle contour. (D) The empty space of the phantoms was filled with contrast medium consisting of 1.0 mmol/L gadolinium diethylenetriaminepentaacetic acid (Gd-DTPA; Magnevist, Schering AG, Berlin, Germany). Transparent plastic wrap was used to hold the contrasting agents in the phantoms.
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Muscle Volume Measurements
The data were analyzed with the use of image-processing software (NIH image 1.62, NIH, US Government, Bethesda, MD, USA) on the Power Macintosh G3 (Apple Computer, Inc., Japan). The images were displayed as a series of 168 contiguous coronal images at intervals of 1.25 mm. The image matrix of 256 pixels x 256 pixels x 168 slices was interpolated to 512 pixels x 512 pixels x 168 slices. This program yields 3D image volume elements (voxels) with 0.45 x 0.45 x 1.25 mm size. The outlines of the muscles were traced on each coronal section, and the volume measurement was based on a count of the number of voxels. The significance of the differences in the muscle volume before and after jaw opening, and between right and left sides, was tested. The ratio of muscle volume change after jaw opening to the volume at jaw closing was calculated from the following formula:
where A is the volume at the jaw-closing position, and B is the volume at the jaw-opening position. The significant differences between the right and left sides were tested.
Statistical analyses were conducted with the Wilcoxon signed-rank test. A level of p < 0.05 was considered to be significant. These tests were done with the use of a statistical analysis software package (Stat View 5.0, Abacus Concepts Inc., Palo Alto, CA, USA).
Phantoms for the Calculation of Measurement Errors
We made phantoms of the masticatory muscles to examine the measurement errors of the MRI data. They were made of acrylic plastic and were cylindrical. The diameter and volume of the inside space of each phantom were approximately those of the muscle. A phantom measured 35 mm on the inside diameter, and 60 mm in length. This was the approximate size of the masseter muscle. The other phantom measured 25 mm on the inside diameter, and 30 mm in length. That was the approximate size of the medial and lateral pterygoid muscles. The MR images of the phantom were recorded in the same way as in the human subjects (Fig. 1D ).
The measurement was repeated 3 times for each phantom. We performed the Wilcoxon signed-rank test to determine whether there were any differences among the three repeated measurements of the traced areas for the each of the MR phantom images.
The relative errors of the volume of the phantom were calculated from the following formula:
where C is the theoretical value of the volume, and D is the value obtained in the MRI analysis.
Cross-sectional Area Measurements
Cross-sectional areas of the lateral pterygoid muscle at the jaw-closing position were traced and measured on coronal images. Next, axial images were reconstructed for masseter and medial pterygoid muscles, and the cross-sectional areas of these images were measured.
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RESULTS
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Phantom Images Used for the Calculation of Measurement Errors
No significant differences were found among the three repeated measurements of the traced areas for the each of the MR phantom images (p > 0.05). The mean relative error was 0.02% for volume of the phantom which was the approximate size of the masseter muscle, and -0.5% for volume with the phantom of the medial and lateral pterygoid muscles.
Muscle Volume and Cross-sectional Areas
The Table shows the volume, the ratio of volume change, and the maximum cross-sectional areas of the muscles. The lateral pterygoid muscle showed a significant difference in volume between jaw-closing and -opening positions (medians 10.4 and 9.6 cm3, respectively, p < 0.01). On the other hand, the masseter and medial pterygoid muscles did not show any significant difference in volume (p > 0.05). The lateral pterygoid muscles showed that the ratio of muscle volume change after jaw opening was a median of -6.7%, while the masseter and medial pterygoid muscles showed 0.7% and 1.8%, respectively. Most of the lateral pterygoid muscles showed a constant tendency in which 17 of the 20 registered a decreased volume after opening. On the other hand, the masseter and medial pterygoid muscles did not show any constant trend in volume change (Fig. 2).
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Table. Median (Interquartile Range) of the Volume at the Jaw-closing and -opening Positions (cm3), the Ratio of Volume Change after Jaw Opening (%), and the Maximum Cross-sectional Areas at the Jaw-closing Position (cm2) of the Muscles in These Subjects
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Figure 2. The ratio of muscle volume change after jaw opening to the volume at jaw closing: (opening – closing) x 100/closing (%). (A) Masseter muscle. (B) Medial pterygoid muscle. (C) Lateral pterygoid muscle. Female subjects, a–e; male subjects, f–j. A positive % indicates a greater volume during opening.
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Three-dimensional reconstruction of the traced masticatory muscles showed the morphological changes visually (Fig. 3).
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Figure 3. A typical three-dimensional reconstruction (surface rendering) of the traced masticatory muscles was made by means of Dr. View/PRO software (AJS Co., Ltd, Tokyo, Japan) on the OCTANE workstation (Silicon Graphics Co., Inc., Mountain View, CA, USA) at a jaw-closing position (A, the teeth in the dental intercuspal position) and at a jaw-opening position (B). Only two-dimensional coronal and lateral views of the three-dimensional reconstruction are shown here. The morphological changes, such as the length and cross-sectional size, can be observed after jaw opening. Moreover, the heterogeneity between and within each muscle is demonstrated.
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DISCUSSION
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MRI is an ideal imaging modality for the analysis of muscles because of its excellent soft-tissue resolution, multiplanar capacity, and lack of any ionizing radiation. In addition, the artifacts from dental restorations are less than on CT analysis. Ultrasonography is non-invasive but examiner-dependent, and it is difficult to measure muscle volume. Previous MRI studies investigated thick slices of images because spin-echo sequences were used (Hannam and Wood, 1989; van Spronsen et al., 1989, 1997; Koolstra et al., 1990; Goto et al., 1995, 2001; Shiau et al., 1999). A problem with this approach is the accuracy of muscle dimensions, especially small muscles such as the lateral pterygoid muscle. In previous studies, the cross-sectional areas of the lateral pterygoid muscles were not very accurate. Only a multi–slice reconstruction of this muscle may solve the problem (van Spronsen et al., 1989).
The 3D MP RAGE Method
We selected 3D magnetization-prepared rapid gradient-echo imaging (the 3D MP RAGE approach and method) to overcome these previous problems. The advantages of the 3D MP RAGE method include a superior T1 contrast, decreased imaging time, decreased motion artifacts, and reduced partial-volume effects when compared with conventional thick-section T1-weighted spin-echo images and the 3D fast low-angle shot studies (Mugler and Brookeman, 1990; Runge et al., 1991). Another important advantage was that this sequence was designed to acquire large 3D data sets with a small voxel size from the entire head, so that the data allowed us to perform off-line (post-study) reconstructions of high-quality images in any desired plane (Mugler and Brookeman, 1991). These advantages made it possible for us to distinguish the muscle from its neighboring muscle and soft tissues.
The mean relative errors were 0.02% and -0.5% for volume measurements with the phantoms. These relative errors seem to be minimal because the phantoms had a regular shape. The relative error was 3.7-5.1% with the phantoms that had shapes similar to those of the masticatory muscles evaluated on CT with slice thickness of 4 mm (Xu et al., 1994). The errors associated with this kind of irregular phantom are supposed to be smaller in our system than in the results previously reported by Xu et al., because of the advantages of the 3D MP RAGE approach. The errors of our system are considered to be acceptable for demonstrating volume changes.
Muscle Volume
The normative values of the muscle volume
The muscle volume should decrease with age. The cross-sectional area and density of the masseter and medial pterygoid muscles show a significant reduction with subject age in the study that involved subjects between 20 and 90 yrs of age (Newton et al., 1993). Taking into account the age of our subjects, our results for the volume of masseter and medial pterygoid muscles at the jaw-closing position were consistent with those from previous studies. The masseter muscle volume in young adults was 31.77 ± 8.99 cm3 (Shiau et al., 1999), and the volume of the masseter and medial pterygoid muscles in older adults was 21.22 ± 6.16 cm3 and 9.32 ± 2.15 cm3, respectively (Xu et al., 1994). When older, somewhat overweight, subjects with Obstructive Sleep Apnea were included, the masseter and medial pterygoid muscles had a mean volume of 30.4 ± 4.1 cm3 and 11.5 ± 2.01 cm3, respectively (Gionhaku and Lowe, 1989).
It was difficult for us to compare the cross-sectional areas of the muscles in our subjects with those from previous reports, because the subjects and methods were different among studies.
The volume changes
This is the first report to quantify the volume changes of the masseter, medial, and lateral pterygoid muscles during jaw opening. We realize the influences of measurement errors and the variation in muscle volume among subjects. However, it is important to emphasize that the most lateral pterygoid muscles showed a constant tendency of decreasing volume after jaw opening.
The physiological reason for the decrease in the volume of lateral pterygoid muscle after jaw opening remains unclear. Some possible explanations for this include: (1) a decrease in the lengths of muscle fibers when the muscle contracts (Huxley, 2000); (2) compression of the lateral pterygoid muscle by the condyle; and (3) changes that may occur in regional blood flow.
Since the lateral pterygoid muscle really consists of both superior and inferior heads, and the inferior head would normally be contracting as one of two major jaw-opening muscles (Grant, 1973; Sessle and Gurza, 1982; Parker, 1983), the volume may reflect the shortening of this head of the pterygoid.
The blood-volume decreases in the human masseter and temporalis muscles were induced even by low levels of isometric contraction (Kim et al., 1999). If the lateral pterygoid muscles during jaw opening in our study were in a similar hemodynamic condition, the decrease in blood-volume could be one of the reasons accounting for decreased muscle volume. With the masseter muscle, the blood volume decreases during muscle extension. However, it recovers with extending time (Inoue-Minakuchi et al., 2001). Our subjects extended their masseter muscle for 6 min during jaw opening, and the decreased blood volume might have been supplemented. The hemodynamic responses were clearly different between the masseter and temporalis (Kim et al., 1999). We realize that blood flow changes due to the force, time, and architecture of muscle. We could not determine the blood flow of the lateral pterygoid muscle, but do believe that the differences in the blood flow are reflected in muscle volumes.
From a morphological standpoint, three-dimensional reconstructed images of the masticatory muscles suggest visually that the length and cross-sectional size of the masticatory muscles may also have changed during jaw opening. The length changes in masseter muscle after jaw movements have already been reported (Goto et al., 2001). However, the other features are still unclear. Our results suggest that the volume changes differ among jaw muscles, which may reflect functional consequences such as force-producing and physiological properties during jaw movement. Further morphological and quantitative studies are important to our understanding of the factors leading to the observed volume changes. We are now developing a new system to investigate the correlation between the changes in the volume and length or the cross-sectional size of the masticatory muscles.
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ACKNOWLEDGMENTS
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We are grateful to Dr. Kazunori Yoshiura and Mr. Makoto Kato for their help with the technical aspects of this project. We thank Prof. Brian Quinn for critically reading the manuscript. This study was supported by a Grant-in-Aid for Scientific Research from the Ministry of Education, Japan (No. 10771033) and the Nakamura Foundation.
Received for publication June 18, 2001.
Revision received March 26, 2002.
Accepted for publication April 18, 2002.
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Journal of Dental Research, Vol. 81, No. 6,
428-432 (2002)
DOI: 10.1177/154405910208100614
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ABSTRACT
INTRODUCTION
