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J Dent Res 84(6):570-575, 2005
© 2005 International and American Associations for Dental Research

RESEARCH REPORT
Clinical

In vivo Cross-sectional Area of Human Jaw Muscles Varies with Section Location and Jaw Position

T.K. Goto1,*, M. Yahagi2, Y. Nakamura3, K. Tokumori1, G.E.J. Langenbach4, and K. Yoshiura1

1 Department of Oral and Maxillofacial Radiology, Faculty of Dental Science, Kyushu University, 3-1-1, Maidashi, Higashi-ku, Fukuoka, 812-8582, Japan;
2 Asahi Kasei Information Systems Co., Ltd., Tokyo, Japan;
3 Department of Radiology, Kyushu University Hospital, Fukuoka, Japan; and
4 Department of Functional Anatomy, Academic Centre for Dentistry Amsterdam (ACTA), Universiteit van Amsterdam and Vrije Universiteit Amsterdam, The Netherlands;

* corresponding author, goto{at}rad.dent.kyushu-u.ac.jp


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS & METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Muscle cross-sectional area (CSA) is used as a measure for maximum muscle force. This CSA is commonly determined at one location within the muscle and for one jaw position. The purpose of this study was to establish a method to standardize the analysis of the CSA of the masticatory muscles in vivo, and to compare the CSAs along their entire length for two different jaw positions (opened and closed). The CSAs in the planes perpendicular to the long axes of the masseter, medial, and lateral pterygoid muscles were measured in ten normal young adult subjects by magnetic resonance imaging. Our results showed large differences among the muscles and a non-uniform change in CSA after jaw-opening. The method enables the CSA measurement to be standardized in vivo, and allows for a correct comparison of CSAs in different skull morphologies.

KEY WORDS: human masticatory muscles • muscle cross-sectional area • magnetic resonance imaging • jaw-opening


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS & METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
The cross-sectional area (CSA) of the masticatory muscles is considered proportional to maximum muscle force (Weijs and Hillen, 1985a, b; van Eijden et al., 1997). Detailed data on the interindividual variation of muscle morphology, such as its length and physiological CSA and force indices, have been reported for the jaw-closed position in cadavers of older individuals (van Eijden et al., 1997), in whom it is known that the CSAs of the masticatory muscles are reduced with age (Newton et al., 1987, 1993).

Investigations of the CSA in living human subjects can be performed by computed tomography (Weijs and Hillen, 1984b), ultrasonography (Emshoff et al., 1999; Bertram et al., 2003), or magnetic resonance imaging (MRI) (Hannam and Wood, 1989; Sasaki et al., 1989; van Spronsen et al., 1989). Although Weijs and Hillen (1984a) and van Spronsen et al.(1989) determined the CSA at several locations along the muscle’s length, the CSA is commonly determined at only one location, i.e., at the visually determined bulge of the muscle (more or less perpendicular to the muscle’s long axis), and for only one jaw position.

Several jaw-closing muscles are known for their complex multi-pennate architecture, while the jaw-openers are much simpler in architecture (van Eijden et al., 1997). So far, it is largely unknown to what extent the CSA varies with the section location and jaw position and orientation. Because of the various muscle orientations, jaw-opening will have a differential impact on the CSA among muscles and, due to the complex internal architecture, possibly also on the CSA changes within muscles.

The purposes of this study were to: (1) establish a method to standardize the analysis of the CSA of each masticatory muscle in vivo, (2) determine the CSAs along the entire length of masticatory muscles (masseter, medial, and lateral pterygoid muscles), and (3) examine the changes in these CSAs after a complete opening motion. We hypothesized that, because of the complex internal architecture of masseter and medial pterygoid muscles, the changes in CSA after jaw-opening would not occur uniformly from origin to insertion. In contrast, the change in CSA would be uniform in the less complex lateral pterygoid muscle.


   MATERIALS & METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS & METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Data Acquisition
The subjects were ten normal Japanese adults, five females and five males, from 20 to 30 yrs of age. All subjects had normal skull shape, normal occlusion, well-arranged dentitions, and no signs of craniomandibular dysfunction. All experimental procedures were approved by the human experimentation committee of Kyushu University. All subjects gave informed consent. In each individual, the masseter, medial, and lateral pterygoid muscles were evaluated by MRI (1.5 Tesla; Magnetom Vision, Siemens AG, Erlangen, Germany; three-dimensional rapid gradient-echo sequence), allowing for the acquisition of a large quantity of three-dimensional high-quality data (voxel size: 0.9 x 0.9 x 1.25 mm). For the first collection of images, the subjects held their teeth loosely together in the intercuspal position. Next, a custom-made acrylic plastic block comfortably kept the jaw at the maximum open position.

The MR data were converted to 168 continuous coronal slices at 1.25-mm intervals. After the pixel size on coronal images was interpolated from 0.9 x 0.9 mm to 0.45 x 0.45 mm, the contours of the muscles were traced on the coronal images with the use of image-processing software (NIH image 1.62, NIH, US Government, Bethesda, MD, USA). Each series of MR images was then reconstructed (Dr. View/LINUX, AJS Co., Ltd., Tokyo, Japan), resulting in three-dimensional data of the entire subject’s head, allowing for the visualization of high-quality images in any desired plane.

CSA Determination
For CSAs in each muscle to be determined correctly, they must be measured at an angle perpendicular to the actual muscle’s long axis (action line). To define this long axis in the masseter and medial pterygoid muscles, one must measure the muscle’s medio-lateral inclination relative to the Frankfort horizontal plane. Therefore, the frontal muscle angles were measured with the use of coronal scans crossing the hypophysis (Fig. 1A-1Go). We then used reconstructed images parallel to the frontal angle and perpendicular to the coronal plane to obtain a ‘lateral view’ of the muscle, to determine its long axis. In each ‘lateral view’ image, the muscle’s midline was determined according to lines describing the posteriormost and anteriormost boundaries. Because these boundaries are curved and shift their position (depending on the muscle’s depth), this midline was estimated for subsequent reconstructed continuous ‘lateral view’ images. Averaging these subsequent midlines provided the long axis in each muscle. After that, the CSAs of masseter and medial pterygoid muscles were determined (Dr. View/LINUX) at 1-mm intervals perpendicular to their respective long axes (Fig. 1A-2Go). The number of sections along the muscle’s long axis is an estimation of the length of the muscle. To ensure a smoothing of errors by margin tracing, we took the mean value of CSA at three contiguous sections as one CSA measurement.



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  		Figure 1. Determination of the cross-sectional areas of the jaw muscles. (A) The determination of cross-sectional areas of the masseter and medial pterygoid muscles. (1) Frontal muscle angles (blue lines) are estimated with the use of coronal scans which cross the hypophysis (yellow line), as indicated by the top mid-sagittal image. (2) Reconstructed ‘lateral view’ images parallel to the frontal angles, and perpendicular to the coronal plane. The muscle’s long axis (green dotted line) was defined as the midline between the anteriormost and posteriormost margins of each muscle on these reconstructed images. The cross-sectional areas (red lines) were determined at 1-mm intervals perpendicular to this muscle’s long axis. (B) The determination of cross-sectional areas of the lateral pterygoid muscle. (1) The axial muscle angle (blue line) was estimated with the use of an axial scan, which showed the maximum area of the lateral pterygoid muscle. (2) Reconstructed images parallel to the axial angle and perpendicular to the axial plane. The muscle’s long axis (green dotted line) was defined as the midline between the superiormost and inferiormost margins of muscle. The cross-sectional areas (red lines) were determined perpendicular to the muscle’s long axis at 1-mm intervals. R, right side; L, left side. MS, masseter muscle; MP, medial pterygoid muscle; LP, lateral pterygoid muscle.

 
For the lateral pterygoid muscle, we used the axial scan to determine the muscle’s axial angle (Fig. 1B-1Go). We then used reconstructed images parallel to this angle and perpendicular to the axial plane to estimate the muscle’s long axis. CSAs were estimated perpendicular to this muscle’s long axis (Fig. 1B-2Go). The CSA estimation of all muscles for the jaw-open position followed the same procedure.

Data Analysis
At the jaw-closed position, we examined (paired t test) possible differences between the left- and right-side muscles by comparing their maximal CSAs and the CSAs along the muscles’ long axes. To compare the CSAs among individuals and for the two different jaw positions, we normalized both the CSAs and the muscle lengths. The relative position of the maximum CSA and its variation among individuals, as expressed by the coefficient of variation (= SD/mean x 100%), were calculated. Averaged absolute (non-normalized) CSAs were computed and plotted against the muscle length, showing differences among muscles and between the two jaw positions. The difference between the maximum absolute CSAs before and after jaw-opening was expressed as a percentage of the CSA at the jaw-closed position.

Differences in relative position and the magnitude of the maximum CSA between the closed and open jaw positions were tested for their significance by the paired t test. The p < 0.05 was considered to indicate a significant difference.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS & METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
A comparison of the right and left muscles at the closed-mouth position did not reveal any statistically significant difference in CSAs. Therefore, to simplify the presentation of the results, we show here only the data for the left muscles.

The normalized individual CSA determinations along the entire muscle’s length among all subjects are presented (Fig. 2Go). In general, at a jaw-closed position, the resulting muscle shapes, as expressed by the successive CSAs, were very comparable among individuals. The dispersion of data-points indicated the variation among subjects. The masseter muscle’s maximum CSA (Fig. 2Go) was variably positioned among individuals (coefficient of variation [COV] = 24.7%). The medial and lateral pterygoid muscles showed, respectively, almost constant (7.3%) and intermediately variable (16.6%) positions of their maximum CSA.



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  		Figure 2. The normalized graphs (for both maximum CSA and muscle length) of the cross-sectional areas in relation to muscle length. The data-points from the left sides of 10 subjects are shown in each graph. Cross-sectional areas at the closed and open jaw positions are shown, respectively, in the left- and right-side panels. The dispersion of data-points indicates the variation in muscle morphology among subjects. The crossbar shows the position at which the maximum CSA (mean) was located. *Significant difference between the closed and open jaw positions (P < 0.001).

 
After jaw-opening, the relative position of maximum CSA of only the lateral pterygoid muscle changed significantly (from 0.42 to 0.54, p < 0.001). The interindividual variation in the position of the maximum CSA was comparable with that of the jaw-closed position (for masseter, medial, and lateral pterygoid muscles, 26.1%, 7.1%, and 10.4%, respectively).

The mean non-normalized CSAs of all 3 muscles along the entire muscle length for both jaw positions are shown (Fig. 3Go). At the jaw-closed position, the masseter muscle increased its CSA over a distance of about 20 mm on both the origin and insertion sites. Along a large portion of the muscle, between 20 mm and 60 mm, its CSA varied between 4.0 and 5.0 cm2, close to the maximal CSA. In contrast, the medial pterygoid muscle was much more fusiform. The lateral pterygoid muscle showed a small plateau in its CSAs (ca. 3.5 cm2) between 15 and 25 mm of its length.



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  		Figure 3. The non-normalized cross-sectional area (mean, n = 10) of masseter, medial, and lateral pterygoid muscles in relation to their total length and for the two examined jaw positions. Masseter, masseter muscle; Medial pterygoid, medial pterygoid muscle; Lateral pterygoid, lateral pterygoid muscle.

 
After jaw-opening, the masseter muscle’s CSAs were decreased inconsistently, mainly in the plateau portion, and its length increased, on average, by 6.1 mm (from 79.2 to 85.3 mm). Note that the calculation of the average CSAs (Fig. 3Go) generates different muscle lengths (92 and 96 mm) that point to the length measurements in the individual with the longest masseter muscle. The medial pterygoid muscle showed a decrease of CSA, mainly at its maximum CSA, and increased its length from 64.0 to 66.4 mm. The lateral pterygoid muscle increased its CSA after jaw-opening, and shortened from 41.9 to 34.0 mm.

The maximum CSA at the jaw-closed position of the masseter muscle was the largest (5.2 cm2), followed by the lateral (3.8 cm2) and medial (3.0 cm2) pterygoid muscles (TableGo). After jaw-opening, the CSA of the masseter and medial pterygoid muscles showed a significant decrease of 11.3% and 14.3% (p < 0.005), while the lateral pterygoid muscle significantly increased its CSA (22.7%, p < 0.005).


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  		Table. Mean ± SD of the Maximum Cross-sectional Areas (CSA) for the Closed and Open Jaw Positions (cm2), and the Ratio of the Maximum CSA Change after Jaw-opening (%) (N = 10)
 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS & METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
Using MRI, we developed a method to estimate the CSA along the entire length of the muscles. This method ensures the standardized determination of the maximum CSA, taking into account individual differences in muscle orientation. It enables these CSAs to be compared between and among various muscles and individuals, and allows for the influence of jaw position to be examined. To our knowledge, this is the first study quantifying the CSAs of masticatory muscles, taking into account the orientation of individual muscles and estimating the changes in the CSA after jaw-opening in living humans. Although some interindividual variation is present, the general shape of these muscles, expressed by the subsequent estimated CSAs, was remarkably constant.

In the jaw-closed position, the maximum CSAs of masseter muscles reported in the present study were comparable with those reported in other studies (Weijs and Hillen, 1985a; Newton et al., 1987, 1993; Gionhaku and Lowe, 1989; Hannam and Wood, 1989; Sasaki et al., 1989; van Spronsen et al., 1989; Xu et al., 1994; Gan et al., 2000). The medial and lateral pterygoid muscles showed CSAs of 3.0 and 3.8 cm2, which are smaller than the previously reported ranges of 3.1 to 3.8 and 4.2 to 4.7 cm2, respectively. A possible explanation is that we analyzed the CSAs of sections perpendicular to the long axes of the muscles, while, in most other studies, the sections were taken parallel to anatomical planes (e.g., Frankfort horizontal, coronal plane, etc.). This might lead to an overestimation, especially for the medial and lateral pterygoid muscles, which have large medio-lateral components in their orientations. In a previous publication, we presented the CSA parallel or vertical to the Frankfort horizontal plane from the same subjects (Goto et al., 2002). These CSAs were indeed larger than those of the current study. Additional reasons for this discrepancy may be related to race, sex, and face morphology. However, previous studies of the CSA of jaw muscles do not reveal a consistent difference between populations. From this, it can be suggested that variations due to population differences are of a lesser magnitude than those due to methodological differences. It is difficult to clarify possible population differences without using standardized methods. The maximum CSAs of masseter, medial, and lateral pterygoid muscles in the current study were closer to the muscle’s insertion than found in the study of Weijs and Hillen (1984a). Moreover, in the study of Weijs and Hillen, the medial pterygoid muscle showed a nearly constant CSA for a large portion of the muscle, while the muscle was fusiform in our study. Comparison with the results of van Spronsen et al.(1989) suggests a difference in the form and length of both the masseter and medial pterygoid muscles. This might be related to the inter-slice interval of 6 mm in that study, making the determination of muscle length difficult.

Our results show that there is variation in muscle form among subjects, among muscles, and within the muscles. In addition, the results indicate that the position at which the maximum CSA is determined is crucial in the medial and lateral pterygoid muscles, whereas, in the masseter muscle, this is inconsequential, due to its broad muscle portion, showing near-maximum CSAs. Nevertheless, the determination of the CSA at only one location of the muscle may not reveal the true maximum CSA. Moreover, in previous studies, scans were simultaneously made for both sides of the masticatory system, and their orientations were according to the estimation within one individual, which was further copied to all examined subjects. The variations in the previously published CSAs reveal that this parameter can differ substantially, depending on the methods and subjects, indicating that a standardized method, taking into account individual differences, as used in the present study, might improve the CSA estimation. Koolstra et al.(1989) published a method that estimated the line of action of muscles as a regression line through the centroids of mathematical slices of muscles. Our method is comparable with that method, since we used a series of midlines to determine the muscle’s action line (long axis).

After jaw-opening, the variation of the normalized muscle contours tends to become larger for the masseter and medial pterygoid muscles at the origin (Fig. 2Go); that is, jaw-opening resulted in a non-uniform decrease in the CSAs of, especially, the masseter muscle and, to a lesser extent, the medial pterygoid muscle, while the lateral pterygoid muscle tended to show a homogeneous increase in its CSAs. This is in agreement with our hypothesis, and relates to the complex internal architecture found in the masseter and medial pterygoid muscles (van Eijden et al., 1997). The length changes in the examined muscles were as expected. Masseter and medial pterygoid muscles elongated after opening, while the lateral pterygoid muscle clearly shortened.

The relative length at which the maximum CSA was found did not change during jaw-opening for the masseter and medial pterygoid muscles. The lateral pterygoid muscle, however, significantly changed its maximum CSA position from 0.42 to 0.54 during opening (Fig. 2Go), probably due to its unmistakable shortening (Fig. 3Go). It seems that the shortening of its length exerted a great influence on the shape of the lateral pterygoid muscle during opening.

In conclusion, our study showed that: (1) the natural CSAs of masticatory muscles changed markedly along their entire length; and that (2) during jaw-opening, the CSAs did not always change uniformly from origin to insertion. As such, these results are valuable for various clinical issues. The method enables us to determine the CSA accurately in a standardized way, taking into account individual differences in muscle orientation, and thus facilitates the comparison of CSAs in children, normal individuals, and patients with jaw and muscle deformities. The results of the present study are also highly relevant to biomechanical studies of the craniofacial region.


   ACKNOWLEDGMENTS
 
We are grateful to Ms. Satoko Nishida for her assistance in the data analysis and to Prof. Theo van Eijden for critically reading the manuscript. We also thank Prof. Brian Quinn, who is expert in the English language, for reviewing the manuscript. This study was supported by a Grant in Aid of Scientific Research from the Ministry of Education, Japan (Nos. 10771033, 12771123, 14571792). A preliminary report of this study was presented at the 81st General Session & Exhibition of the International Association for Dental Research, 2003, held in Göteborg, Sweden.

Received July 15, 2004; Last revision March 30, 2005; Accepted March 31, 2005


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS & METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Bertram S, Bodner G, Rudisch A, Brandlmaier I, Emshoff R (2003). Effect of scanning level and muscle condition on ultrasonographic cross-sectional measurements of the anterior masseter muscle. J Oral Rehabil 30:430–435.[ISI][Medline]

Emshoff R, Bertram S, Strobl H (1999). Ultrasonographic cross-sectional characteristics of muscles of the head and neck. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 87:93–106.[ISI][Medline]

Gan Y, Sasai T, Nishiyama H, Ma X, Zhang Z, Fuchihata H (2000). Magnetic resonance imaging of human mandibular elevator muscles after repetitive maximal clenching exercise. Arch Oral Biol 45:247–251.[ISI][Medline]

Gionhaku N, Lowe AA (1989). Relationship between jaw muscle volume and craniofacial form. J Dent Res 68:805–809.[Abstract/Free Full Text]

Goto TK, Tokumori K, Nakamura Y, Yahagi M, Yuasa K, Okamura K, et al. (2002). Volume changes in human masticatory muscles between jaw closing and opening. J Dent Res 81:428–432.[Abstract/Free Full Text]

Hannam AG, Wood WW (1989). Relationships between the size and spatial morphology of human masseter and medial pterygoid muscles, the craniofacial skeleton, and jaw biomechanics. Am J Phys Anthropol 80:429–445.[ISI][Medline]

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T.K. Goto, S. Nishida, M. Yahagi, G.E.J. Langenbach, Y. Nakamura, K. Tokumori, S. Sakai, H. Yabuuchi, and K. Yoshiura
Size and orientation of masticatory muscles in patients with mandibular laterognathism.
J. Dent. Res., June 1, 2006; 85(6): 552 - 556.
[Abstract] [Full Text] [PDF]

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