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Size and Orientation of Masticatory Muscles in Patients with Mandibular Laterognathism

¹ Department of Oral and Maxillofacial Radiology, Faculty of Dental Science, Kyushu University, 3-1-1, Maidashi, Higashi-ku, Fukuoka, 812-8582, Japan;
² Faculty of Dental Science, Kyushu University, Fukuoka, Japan;
³ Asahi Kasei Information Systems Co., Ltd., Tokyo, Japan;
⁴ Department of Functional Anatomy, Academic Centre for Dentistry Amsterdam (ACTA), Universiteit van Amsterdam, and Vrije Universiteit Amsterdam, Netherlands;
⁵ Department of Medical Technology, Kyushu University Hospital, Fukuoka, Japan; and
⁶ Department of Clinical Radiology, Graduate School of Medical Sciences, Kyushu University, Fukuoka, Japan

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

	ABSTRACT

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Size measurements of jaw muscles reflect their force capabilities and correlate with facial morphology. Using MRI, we examined the size and orientation of jaw muscles in patients with mandibular laterognathism in comparison with a control group. We hypothesized that the muscles of the deviated side would be smaller than those of the non-deviated side, and that the muscles of both sides would be smaller than in controls. In patients, a comparison of deviated and non-deviated sides showed, in orientation, differences for masseter and medial pterygoid muscles, but, in size, differences only for the masseter muscle. Nevertheless, muscle sizes in patients were much smaller than in controls. Lateral displacement of the mandible can explain the orientation differences, but not the smaller muscle size, in patients. It is possible that the laterodeviation initiates an adaptive process in the entire jaw system, resulting in extensive atrophy of the jaw muscles.

Key Words: human masticatory muscles • muscle cross-sectional area • muscle orientation • magnetic resonance imaging • mandibular laterognathism

	INTRODUCTION

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The size (cross-sectional area, length, and volume) of human jaw muscles varies with craniofacial form. It has been shown that the cross-sectional area of jaw muscles, which reflects their force capabilities, is correlated to facial morphology (Weijs and Hillen, 1984, 1986). Long-face adults have masticatory muscles with small cross-sectional areas, which relate to the lower bite-force magnitudes found for these subjects (Kiliaridis and Kälebo, 1991; van Spronsen et al., 1992). Also, subjects with mandibular prognathism show smaller cross-sectional areas (Ariji et al., 2000) or volumes (Kitai et al., 2002) of jaw muscles.

The orientation of jaw muscles has been studied in subjects with normal craniofacial form, in comparison with long- and short-face subjects. Jaw muscle orientation seems to be related to variations in facial height and mandibular shape (gonial angle) (van Spronsen et al., 1997). The jaw muscles in long-face subjects have been reported to be more obliquely oriented compared with those in normal or short-face subjects (Takada et al., 1984; Haskell et al., 1986); however, another study found no differences (van Spronsen et al., 1996).

In the case of facial asymmetry, there are several studies on muscle size in hemifacial microsomia, a congenital craniofacial malformation. A recent publication (Huisinga-Fischer et al., 2001) showed that, in hemifacial microsomia, the jaw muscles of the non-affected side were less developed than those of controls. In addition, a comparison of both muscle sides within patients showed that muscles were significantly smaller on the affected than on the unaffected side (Kahl-Nieke and Fischbach, 1998; Takashima et al., 2003; Huisinga-Fischer et al., 2004). It seems that the degree of hypoplasia of the masticatory muscles in these patients increases with the degree of mandibular dysmorphology (Marsh et al., 1989; Kane et al., 1997). Subjects with mandibular laterognathism (Maki et al., 2001), a non-congenital craniofacial asymmetry, showed bilateral differences in the size of the masseter muscle. These differences in size can be the result of a simple relocation of the mandible, or caused by a change in the jaw system, generating, for instance, asymmetry in all jaw muscles. In the first case, one would expect the size of the jaw muscles to be basically the same in patients and controls. In the latter case, the jaw muscles will show clear size differences, which could affect one muscle more than another.

So far, the relationship between the size and the orientation of the jaw muscles and mandibular laterognathism remains unclear. Also, it is unresolved how muscle size and orientation in patients relate to normal subjects. Using a previously published method of muscle size determination (Goto et al., 2005a), we examined the jaw muscles in patients with mandibular laterognathism and compared them with those in controls.

The purposes of this study were to investigate the differences in size measurements (cross-sectional area, length, and volume) and orientation of the masticatory muscles between deviated and non-deviated sides of the jaw in patients with mandibular laterognathism, and to compare these parameters with values obtained in controls. It was hypothesized that the jaw muscles of the deviated side would be smaller and oriented differently from those of the non-deviated side, and that the muscle sizes would be smaller than those in controls.

	MATERIALS & METHODS

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Subjects
The study was carried out in 20 patients randomly chosen from a group of 27 with skeletal mandibular laterognathism and who were planning to undergo orthognathic surgery: ten females and ten males, 16–28 yrs of age (21.3 ± 3.4 yrs). Both the left and right sides of the masseter, and the medial and lateral pterygoid muscles were analyzed. The deviation between the midline of the upper and lower incisors ranged, at a closed-jaw position, from 3 to 11 mm (mean, 5.6 ± 1.9 mm). The maxilla did not show deviation, and we defined ’deviated side’ as the side of midline shift of the mandible. None of the patients had a known congenital disease, a history of injury, tumors, overgrowth in one condyle, or was receiving orthodontic therapy (Goto et al., 2005b). The controls were ten adults: five females and five males, 20–30 yrs of age. All controls had normal skull shape, normal occlusion, well-arranged dentitions, and no signs of craniomandibular dysfunction. Informed consent was obtained from each of the participants. The Human Experimentation Committee of Kyushu University approved all experimental procedures, and all participants gave informed consent.

Data Acquisition
The muscles were evaluated by MRI (1.5 Tesla; voxel size 0.9 x 0.9 x 1.25 mm; Magnetom Vision, Siemens AG, Erlangen, Germany). The participants held their teeth loosely together in the intercuspal position. During imaging, the participants were monitored by a camera as a control for their mandibular posture. The contours of the muscles were traced on the frontal images and were then reconstructed, resulting in a three-dimensional dataset of the participant’s entire head, showing the individual jaw muscles (NIH Image 1.62; US NIH, Bethesda, MD, USA). The reconstruction allowed for the visualization of the images in any desired plane (Dr. View/Linux, AJS, Tokyo, Japan). Cross-sectional areas were measured at an angle perpendicular to the actual muscle’s long axis. For a detailed description of the method, see Goto et al.(2005a). In brief, to define the long axis in the masseter and medial pterygoid muscles, we measured the frontal angle of the muscle relative to the Frankfort horizontal plane. We then used reconstructed images parallel to this angle and perpendicular to the frontal plane to obtain a ’lateral view’ of these muscles to determine the long axis. Subsequently, a series of cross-sectional areas was determined at 1-mm intervals perpendicular to the long axis. For the lateral pterygoid muscle, we used axial scans to determine the muscle’s axial angle. Reconstructed images parallel to this angle and perpendicular to the axial plane were then used to estimate the muscle’s long axis. Cross-sectional areas were determined at 1-mm intervals perpendicular to this muscle’s long axis.

We used the number of sections along the muscle’s long axis to estimate the length of the muscle. We used the number of voxels within the reconstructed muscles to calculate the muscle volume.

The orientation of each of the muscle’s long axes was described by 2 angles. For the masseter and medial pterygoid muscles, the frontal and sagittal angles between the muscle’s long axis and the Frankfort horizontal plane were used. For the lateral pterygoid muscle, the axial and sagittal angles were used (Fig. 1).

View larger version (74K): [in this window] [in a new window]   Figure 1. Methods in size measurements (cross-sectional area, length, and volume) and orientation of the masticatory muscles. (A) Reconstruction of MR images and individual jaw muscles: masseter (green), medial pterygoid (orange), and lateral pterygoid (red). Two different participants are shown, with the patient on the left as an experimental subject and the control on the right. (B) Reconstructed images showing the sagittal angle of the right jaw muscles. Horizontal lines are parallel to the Frankfort horizontal plane. Oblique lines represent the long axes of the muscles. Angle between the two lines describes the sagittal orientation of the muscles. (C) Coronal (masseter and medial pterygoid) and axial (lateral pterygoid) scans, showing the orientation in the respective planes. Horizontal lines are parallel to the Frankfort horizontal plane. Abbreviations: MS, masseter muscle; MP, medial pterygoid muscle; LP, lateral pterygoid muscle.

	RESULTS

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Muscle Size
In patients, only the masseter muscle showed a significantly smaller length and volume on the deviated side than on the non-deviated side. Maximum cross-sectional area was not different between both sides for any of the muscles (Fig. 2, left panels). However, the sizes of the jaw muscles were clearly smaller in patients than in the controls. In patients, the masseter showed smaller maximum cross-sectional areas (3.9 and 4.0 cm² for deviated and non-deviated sides, respectively), compared with the control group (5.3 cm²), and much smaller volumes, in particular (16.9 and 18.2 cm³ for deviated and non-deviated sides, respectively) than in the controls (29.8 cm³). A similar but less extreme result was found for the medial pterygoid, whereas the lateral pterygoid muscle showed only a smaller volume. The length of the muscles showed no difference between the patient and control groups.

View larger version (34K): [in this window] [in a new window]   Figure 2. Maximum cross-sectional areas (cm2), muscle length (mm), muscle volume (cm3), and orientations (°) of masseter, medial, and lateral pterygoid muscles, respectively. Patient group, n = 20, for each deviated or non-deviated side of 20 patients; control group, n = 10 (mean of both sides of 10 people). Dev, deviated side; Non-dev, non-deviated side. *p < 0.05 by t test with Bonferroni. **p < 0.01 by t test with Bonferroni. p < 0.01 by paired t test with Bonferroni. Significant differences between each side in patients and controls were seen. A marked difference in muscle volume is evident. Abbreviations: CSA, maximum cross-sectional area (cm2); Length, muscle length (mm); Volume, muscle volume (cm3); Angle, orientation (°).

View larger version (29K): [in this window] [in a new window]   Figure 3. Normalized graphs (for both maximum cross-sectional area and muscle length) of cross-sectional areas in relation to muscle length. Data points for 20 muscles from both sides of 10 control participants are shown in the right panel. Data points for each deviated or non-deviated side of 20 participants are shown in the left panels. The dispersion of data-points indicates the variation in muscle morphology among participants. The crossbar shows the position at which the maximum cross-sectional area (mean) was located. Numbers in parentheses show the coefficient of variation (COV = SD/mean x 100%) of the relative position of the maximum cross-sectional area.

	DISCUSSION

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This study reports on the size and orientation of the jaw muscles in patients with non-congenital mandibular laterognathism, and compares these parameters with a representative group of control individuals. A previously published analytical method (Goto et al., 2005a) was used in the investigation. This method facilitates the analysis of muscle cross-sectional areas and lengths independent of facial shape, since it uses, as a reference, the orientation of each muscle, instead of a general reference, such as the occlusal plane or the Frankfort horizontal plane. The total error of our analytical system for muscle volume was less than 0.5% (Goto et al., 2002). This includes the partial volume effect, which is relatively larger in small muscles than in large muscles.

Differences between deviated and non-deviated sides were found only for the masseter, which was slightly shorter and smaller in volume on the deviated side. There was no significant difference in maximum cross-sectional area between the muscles on the deviated and non-deviated sides. The only study on muscle cross-sectional areas in post-natally acquired asymmetrical mandibles (Maki et al., 2001) showed a clear difference in masseter cross-sectional area, contrary to our results. Possible reasons for this discrepancy could be the difference in the participants’ ages. More importantly, the cross-sectional area in their study was measured with one axial cross-section through the middle of the muscle, parallel to the Frankfort horizontal plane. Such a cross-sectional area measurement does not take into account individual variations in facial shape. Thus, the cross-sectional areas are largely influenced by variations in muscle orientation relative to these artificial planes. The present study shows that there are indeed large left-right orientation differences in the masseter muscle.

When patient muscles on both sides were compared, the orientations of the masseter and medial pterygoid muscles were found to be different. These orientation differences can be explained by the laterodeviation of the mandible. In a frontal view, such a lateral position would cause the masseter and medial pterygoid muscles, on the deviated side, to orient more and less vertically, respectively.

In patients, the cross-sectional area and volume of the masseter and medial pterygoid muscles were clearly smaller than in controls, while the lateral pterygoid muscle showed no cross-sectional area difference. Similarly, the orientation of the masseter and medial pterygoid was clearly affected by the mandibular laterognathism—an effect less present for the lateral pterygoid.

The large decreases in muscle sizes described in this study cannot be attributed to the displacement of the mandible alone. Apparently, lateral displacement of the mandible initiates an adaptive process in the entire jaw system, resulting in extensive atrophy of the jaw muscles compared with the normal situation. Smaller jaw-closers were also found in long-face adults (van Spronsen et al., 1992; Ariji et al., 2000). The cross-sectional areas of masseter and medial pterygoid muscles showed a good correlation with bite force (Sasaki et al., 1989; van Spronsen et al., 1989; Raadsheer et al., 1999); therefore, it can be assumed that the smaller cross-sectional areas found in our study are correlated to a weaker bite force. However, it remains unresolved whether this decreased muscle function causes the craniofacial malformation (Kiliaridis, 1995), or vice versa. Although jaw muscle size has been correlated to facial morphology (Weijs and Hillen, 1984, 1986), other functional and epigenetic factors may play an important role (Herring, 1993). Animal studies have shown the association between an experimentally altered oral function and craniofacial development (Hohl, 1983; Nakano et al., 2004). Intriguingly, after full development of the asymmetrical mandible in humans, the asymmetrical distribution of bone mineralization found during development decreases. This finding may suggest that the craniomandibular muscles develop a new equilibrium within the asymmetrical skeleton (Maki et al., 2001).

Interestingly, the lateral pterygoid muscle, which showed the least difference in size and orientation, due to mandibular laterognathism, has no correlation with facial dimensions in normal subjects (Weijs and Hillen, 1984). It is known that the development of the sphenoid bone (origin of the lateral pterygoid muscle) and face width are completed earlier, and that, in adolescence, their growth rate is lower than that of the mandible (Waitzman et al., 1992; Sgouros et al., 1999). Therefore, the lateral pterygoid muscle could be less influenced by asymmetrical morphological change of the mandible in adolescence.

The general shape of muscles was constant among the controls, and that of deviated and non-deviated sides in patients. Nevertheless, it is clear that the variations are larger in patients than in controls, especially for masseter and medial pterygoid muscles, as illustrated by the wider scatter of points in Fig. 3. This suggests that, in patients, the variation of muscle shape may be larger than in controls (Ingervall and Helkimo, 1978). The variation can also be caused by the complex muscle outlines in the patient group (Takashima et al., 2003).

In conclusion, our results showed that (1) in patients, only the masseter showed a smaller muscle size (length and volume) on the deviated compared with the non-deviated side, (2) muscle size (cross-sectional area and volume) in patients was smaller than in controls, and (3) inter-individual variations of muscle shape were larger in patients than in controls. Our standardized method, which takes muscle orientation into account, is useful in comparing cross-sectional areas for different skull morphologies.

	ACKNOWLEDGMENTS

 
We are grateful to Yuko Nakamura, Faculty of Dental Science, Kyushu University, for her assistance in data analysis, and to Professor Theo van Eijden, Department of Functional Anatomy, Academic Centre for Dentistry Amsterdam (ACTA), for critically reading the manuscript. Expert statistical advice was provided by Tomomi Yamada of the Department of Medical Information Science, Kyushu University Hospital, and by Professor Masashi Sugisaki, Department of Dentistry, Jikei University School of Medicine. We also thank the radiological technologists of the Department of Medical Technology, Kyushu University Hospital, for their support in the MR examinations, and Hitomi Nibe, Kyushu University, for her secretarial work. This study was supported by a Grant-in-Aid for Scientific Research from the Ministry of Education, Japan (No. 16591887) and by the Kyushu University Foundation.

Received for publication June 16, 2005. Revision received January 3, 2006. Accepted for publication March 1, 2006.

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Journal of Dental Research, Vol. 85, No. 6, 552-556 (2006)
DOI: 10.1177/154405910608500614


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