Magnetic resonance imaging texture analysis of unilateral lateral pterygoid myospasm in patients with temporomandibular joint disorders: A pilot study

Chenxi Li; Xu Liu; Baihetinuer Muhetaer; Sakendeke Jumatai; Zhongcheng Gong

doi:10.4103/digm.digm_31_21

ORIGINAL ARTICLE

Year : 2021 | Volume : 7 | Issue : 1 | Page : 2

Magnetic resonance imaging texture analysis of unilateral lateral pterygoid myospasm in patients with temporomandibular joint disorders: A pilot study

Chenxi Li¹, Xu Liu¹, Baihetinuer Muhetaer², Sakendeke Jumatai³, Zhongcheng Gong¹
¹ Department of Oral and Maxillofacial Oncology Surgery, Xinjiang Medical University Affiliated First Hospital; School of Stomatology, Xinjiang Medical University; Stomatological Research Institute of Xinjiang Uygur Autonomous Region, Urumqi, Xinjiang, China
² MRI Units, Medical Imaging Center, Xinjiang Medical University Affiliated First Hospital, Urumqi, Xinjiang, China
³ School of Stomatology, Xinjiang Medical University; Stomatological Research Institute of Xinjiang Uygur Autonomous Region; Department of Oral and Maxillofacial Radiology, Xinjiang Medical University Affiliated First Hospital, Urumqi, Xinjiang, China

Date of Submission	25-Jul-2021
Date of Decision	10-Aug-2021
Date of Acceptance	23-Aug-2021
Date of Web Publication	07-Dec-2021

Correspondence Address:
Chenxi Li
Department of Oral and Maxillofacial Oncology Surgery, Xinjiang Medical University Affiliated First Hospital, Urumqi 830054; School of Stomatology, Xinjiang Medical University, Urumqi 830011; Stomatological Research Institute of Xinjiang Uygur Autonomous Region, Urumqi 830054
China
Zhongcheng Gong
Department of Oral and Maxillofacial Oncology Surgery, Xinjiang Medical University Affiliated First Hospital, Urumqi 830054; School of Stomatology, Xinjiang Medical University, Urumqi 830011; Stomatological Research Institute of Xinjiang Uygur Autonomous Region, Urumqi 830054
China

Source of Support: None, Conflict of Interest: None

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DOI: 10.4103/digm.digm_31_21

Abstract

Background and Purpose: Lots of clinical observations have found that there is a close relationship between the pathological changes of lateral pterygoid muscle (LPM) and temporomandibular disc displacement. On medical images, unfortunately, these occult dysfunctions of LPM could scarcely be detected by naked eyes. As the presence of intrinsic properties of the human body, textural feature is capable to effectively discover the subtle functional changes of involved tissues. This study aimed to evaluate the lateral pterygoid myospasm in patients with temporomandibular joint disorders (TMD) applying magnetic resonance imaging (MRI) texture analysis. Patients and Methods: From December 2019 to October 2020, totally nine patients suffered from unilateral spasm of LPM (which is a subtype of TMD) were evaluated by MRI, who were consecutively recruited from Xinjiang Medical University Affiliated First Hospital. Gray-level co-occurrence matrix method was used to analyze the textural features of MRI T2-weighted images with the maximum area of LPM scanned at axial (closed-mouth) plane. Independent samples t-test was performed to compare the relevant parameters of bilateral LPMs (healthy- and affected-side of one individual self-controlled trial). Results: There were no statistically significant values between the two sides of angular second moment, inversed differential moment, and entropy (P > 0.05). The contrast of the healthy-side (267.983 ± 45.952) was significantly higher than that of the affected-side (210.003 ± 29.613) (P < 0.05); and the autocorrelation of the healthy-side (4.536 ± 0.819) was significantly lower than that of the affected-side (6.563 ± 1.653) (P < 0.05). Conclusion: The texture contrast and autocorrelation have certain clinical meanings of diagnosis since they could identify the altered status of LPM, and could be considered as the efficient imaging biomarkers to assess LPM changes in patients with TMD.

Keywords: Entropy, Magnetic resonance imaging, Spasm of lateral pterygoid muscle, Temporomandibular joint disorders, Textural feature

How to cite this article:
Li C, Liu X, Muhetaer B, Jumatai S, Gong Z. Magnetic resonance imaging texture analysis of unilateral lateral pterygoid myospasm in patients with temporomandibular joint disorders: A pilot study. Digit Med 2021;7:2

How to cite this URL:
Li C, Liu X, Muhetaer B, Jumatai S, Gong Z. Magnetic resonance imaging texture analysis of unilateral lateral pterygoid myospasm in patients with temporomandibular joint disorders: A pilot study. Digit Med [serial online] 2021 [cited 2023 Jun 8];7:2. Available from: http://www.digitmedicine.com/text.asp?2021/7/1/0/331949

Introduction

It is well-known that temporomandibular joint disorders (TMD) are a kind of clinical syndrome characterized by its self-limitation to some extent. Dystonia of stomatognathic system, as a common pathogeny of TMD, mainly shows facial grimacing, involuntarily repetitive jaw movement, or tongue dyskinesia. No sooner the masticatory muscles are involved, than people always suffer with abnormal opening/closing track of mouth, mandible movement deviation, or a combination of the two anomalies.^[1] Masticatory muscles are comprised of masseter muscle, temporalis muscle™, medial pterygoid muscle, and lateral pterygoid muscle (LPM). Among them, the first threes are in charge of mandible elevation and mouth closing, and their morphometric changes resulted from edemata are associated with pain-related TMD.^[2],[3]

As the only mandibular descending muscle of oromandibular system, LPM plays a crucial role in the chewing cycle. Anatomically, LPM made up of two bellies (a superior belly and an inferior belly) has a triangular shape with quite symmetrical margins.^[4] Both superior and inferior bellies run to temporomandibular joint (TMJ) posteriorly and laterally, presenting: The distal end of the superior belly inserted into the articular disc and capsule along anteromedial edge of mandibular condyle while the distal insertion of the inferior belly is at the neck of the mandibular condyle and in the pterygoid fossa.^[3],[5] It is the sophisticated structure of LPM that determines its special biofunction in mandibular movement, that is, every time the mandible leaves the intercuspal position/centric occlusion, LPM will pull the condyle ahead, and even the slightest forward movement could also involve it.^[6] Myospasm is one type of masticatory muscle disorders (additionally including local myalgia, myofascial pain, myofibrotic contracture, and myositis),^[7] manifesting a series of characteristics such as immediate continuous muscular contraction, causing local pain, limitation of movement,^[8] and increased electromyogram activity.^[9] Given its unique effect in lowering mandibular movement and assisting mouth opening, the LPM is more prone to be affected spasm than other masticatory muscles.

Magnetic resonance imaging (MRI) has become the gold standard for the diagnosis of TMD^[10] due to its good acuity in soft-tissue resolution, which can clearly display the structural characteristics of various parts of TMJ.^{[11],[12],[13]} However, the available scientific literature studying on masticatory myospasm-induced TMD is few, and lateral pterygoid myospasm-related TMD is quite rare on one hand. On the other hand, by conducting MRI examination, D'Ippolito et al.^[14] and Stimmer et al.^[15] successively confirmed that only a small number of TMD patients could be recognized their morphological alterations of LPM; Less than 5% TMD patients with clinical symptoms were detected the lesion of a small amount of muscular parenchyma and tendo. Hence, the diagnostic value of MRI for the observation of lesion of LPM is very limited in some patients whose morphological or signal alterations inconspicuous.

Textural features are the inherent natures of organic tissues of human beings extracted texture descriptors from medical images, which can efficiently reflect slight biofunctional alterations of lesional tissue.^[16] Texture feature analysis, a quantitative approach, can provide a relatively accurate data to detect pathological tissue; moreover, it had been widely applied in astroglioma,^[17],[18] muscular dystrophy,^[19] epilepsia,^[20],[21] amnestic mild cognitive impairment and mild Alzheimer disease,^[22] medication-overuse headache,^[23] and Attention-Deficit/Hyperactivity Disorder classification.^[24] Notwithstanding, texture feature analysis of MRI was not performed in spasm of LPM so far.

The aim of this study was to analyze the textural characteristics concerning on lateral pterygoid myospasm-induced TMD by investigating the resting-state functional MRI materials using gray level co-occurrence matrix (GLCM) technology, which might be the objective imaging basis for the diagnosis of LPM spasm.

Patients and Methods

Study design

We designed a cross-sectional retrospective study. All patients were recruited from the Temporomandibular Joint Specialist Clinic, the First Affiliated Hospital of Xinjiang Medical University, China, between December 2019 and October 2020. The protocol of study was approved by the Ethics Committee, Stomatological School of Xinjiang Medical University, The First Affiliated Hospital of Xinjiang Medical University, and followed the principles outlined in the declaration of Helsinki. Informed consents were signed by all their families. All the data generated or analyzed during this study are included in this published article.

According to the American Academy of Orofacial Pain (AAOP) guidelines for masticatory muscle spasm^[25] combined with Research Diagnostic Criteria for Temporomandibular Disorders,^[26] the diagnostic key points of spasm of LPM are: (a) Onset of dull pain that is confined to deep part of TMJ and its affiliated tissues (e.g., the posterosuperior facet of maxillary tuberosity) at rest and with function; (b) the active maximum opening-degree is <40 mm, the maximum passive opening-degree is 5 mm more than the active opening-degree; (c) the mandible inclines to the affected side when opening the mouth; (d) acute malocclusion in serious LPM spasm cases.

Subject preparation

The inclusion criteria were as follows: (a) patients, who suffered from spasm of LPM, had not accepted any previous treatment; (b) sensation of muscular cramp or tightness via physical palpation; (c) pain was located in the deep TMJ as well as posterior and superior part of maxillary tubercle; (d) mandibular movement dysfunction; (e) the general condition was acceptable for the plain and enhanced MRI examination of bilateral TMJs.

Patients who met any of the following criteria should be excluded: (a) radiological examination showed organic lesions in TMJ; (b) patients had a history of oromaxillofacial infection, trauma, and tumor involved in TMJ; (c) patients had developmental or acquired neuromuscular deficit, rheumatism, rheumatoid arthritis (OA), and other systemic diseases affected TMJ previously; (d) patients presented congenital cranio-maxillo-facial anomalies (e.g., condylar hypertrophy); (e) individuals had accepted orthodontic and orthognathic treatment before; (f) the quality of MRI images was too poor to measure; contra-indications of MRI examination.

Magnetic resonance imaging material acquisition

All subjects underwent the resting-state functional MRI examination of bilateral TMJs, keeping a supine position that Frankfurt horizontal plane was perpendicular to the patient table surface as well as scanning at the oblique sagittal (wide-open and closed mouth), axial (wide-open and closed mouth), and coronal (closed-mouth) planes that the projection angle was in line with the Schüller's position. Their images were evidenced in a 3.0T MR equipment (MAGNETOM Aera, Siemens Healthineers, Erlangen, Germany) set up with circular polarized array coil for total image matrix. For the sequences, T1-weighted fast spoiled gradient recalled echo (T1W-FSGRE) and fast low-angle shot (T1W-FLASH), T2-weighted turbo spin echo (T2W-TSE), diffusion weighted imaging (DWI), and proton density weighted imaging (PDWI) generating contiguous section, respectively, of 20 axial, 15 coronal, and 18 sagittal slices, were used to perform different segments and individual TMJ creation. The technical parameters were listed, such as below, T1W-FSGRE: TR (repetition time) = 700 ms, TE (echo time) = 10 ms, flip angle = 120°, FOV (field of view) = 25.6 cm × 25.6 cm, Matrix = 256 trixy, NEX (number of acquisition) = 1, slice thickness = 2 mm, slice gap = 0.2 mm; T1W-FLASH: TR/TE = 225 ms/11 ms, flip angle = 15°, FOV = 14 cm × 14 cm, Matrix = 256 trixy, NEX = 2, slice thickness = 3 mm, slice gap = 0.2 mm; T2W-TSE: TR/TE = 3600 ms/92.5 ms, flip angle = 120°, FOV = 21 cm × 21 cm, Matrix = 320 × 288, NEX = 2, slice thickness = 3 mm, slice gap = 4 mm; DWI: TR/TE = 3000 ms/64 ms, flip angle = 120°, FOV = 14 cm × 14 cm, Matrix = 500 tri × 8, NEX = 2, slice thickness = 2 mm, slice gap = 0.2 mm; PDWI: TR/TE = 2423 ms/30 ms, flip angle = 120°, FOV = 14 cm × 14 cm, Matrix = 288 × 192, NEX = 2, slice thickness = 2 mm, slice gap = 1 mm. All imaging protocols were identical for all subjects. All MR images were analyzed by two clinicians (a radiologist and an oral and maxillofacial specialist) together.

Magnetic resonance image processing and textural feature analysis

Picture archiving and communication system workstation output the MRI data. All MRIs in DICOM format were processed using ImageJ software version 1.52 (National Institutes of Health, Bethesda, Maryland, USA) (https://imagej.nih.gov/ij) to circle the two bellies of LPM at the oblique sagittal T2 weighted image of closed-mouth position [Figure 1].

Figure 1: Magnetic resonance images of lateral pterygoid muscles at the oblique sagittal plane (mouth closing position). The red and yellow arrows respectively referred to the upper belly and the lower belly of lateral pterygoid muscle in the same patient (a: normal side of temporomandibular joint region; b: pathological side of temporomandibular joint region).

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After converting the raw images to 16-bit images using 16-bit Histogram plugin of ImageJ, on the axial T2W-TSE with closed-mouth position, we extracted the region of interests (ROIs) of LPMs of both healthy and abnormal-side in one patient simultaneously to calculate the maximal area based on GLCM method with GLCM plugin of ImageJ [Figure 2]. In order to avoid the closely adjacent fatty and bony components, freehand selection was used to draw the ROIs on the LPMs slice with maximum area. The GLCM parameters were as follows: Set the size of step in pixels = 1, the direction of step = 0° in advance; angular second moment (ASM), inversed differential moment (IDM), entropy, contrast, and autocorrelation were measured.^[23],[27] The ROIs were placed for three times through the same clinician by the same LPM slice, and the mean value of texture data was regarded as the final result.

Figure 2: The profiles of bilateral lateral pterygoid muscles were delineated to perform textural feature measurement. Circle 1 and 2 indicated the region of interests of pathological lateral pterygoid muscle and normal lateral pterygoid muscle respectively (a: axial view of right lateral pterygoid muscle spasm; b: axial view of left lateral pterygoid muscle spasm).

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Statistics analysis

Statistical analysis was performed by the Statistical Package for the Social Sciences (IBM SPSS version 26.0, New York, USA). Kolmogorov–Smirnov (K-S) test was used to verify the normality of all data, and the normal distribution data was expressed as mean ± standard deviation (SD). All textural data of normal side of LPM was compared with that of affected side by independent-samples t-test. For the sake of comparison, P < 0.05 was considered statistically significant.

Results

Totally, nine patients suffered with unilateral lateral pterygoid myospasm were included in this study. Among them, there existed three cases had articular disc displacement concomitantly [Figure 3]. All patients were aged 13–68 years with an average of 44.125 ages. 244, and these cases had a female:male ratio of 2:1 (six females, three males), presenting there was no significant difference for age (R = 0.101, P = 0.813) and sex (χ² = 1, P = 0.536) between normal and affected sides of LPM of patients. Detailed clinical information is summarized in [Table 1].

Table 1: Clinical information of the included patients.

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K-S test result showed that the MRI textural feature data conformed to the Gaussian distribution (significant >0.05), indicating Independent-Samples t-test was appropriate to calculate the comparison between normal side and affected side of LPMs.

The results of the comparison of the MRI textural features for both normal side and affected side of patients with lateral pterygoid myospasm turned out to be that, there were no statistically significant values between the two sides of ASM, IDM and entropy (P > 0.05). The contrast of the normal side (267.983 ± 45.952) was significantly higher than that of the affected side (210.003 ± 29.613) (P = 0.010); and the autocorrelation of the normal side (4.536 ± 0.819) was significantly lower than that of the affected side (6.563 ± 1.653) (P = 0.008) [Table 2].

Table 2: Comparison of the magnetic resonance imaging textural features for both normal side and affected side of patients with lateral pterygoid myospasm.

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Figure 3: The magnetic resonance images of patients suffered from lateral pterygoid muscle spasm along with articular disc displacement concomitantly. A and C were from the same patient with left lateral pterygoid myospasm and ipsilateral disc displacement simultaneously; B and D were for the right side (blue arrows pointed at the displaced discs; and the green arrows pointed at the spasmodic lateral pterygoid muscles).

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Discussion

The LPMs located bilaterally in infratemporal fossa almost participate in all mandibular movements,^[6] especially are significantly correlated with the temporomandibular disc displacement.^[28] Consequently, not only do LPMs play an essential role in maintaining the stability of TMJ motion, LPMs will also give rise to dysfunction of mandibular movement when spasm occurs, which seriously influence the quality of life of patients. Cao et al.^[1] conducted a retrospective study on 18 patients with lateral pterygoid myospasm and reported that three characteristic signs and symptoms (concluding as: (a) difficulty in jaw closing after wide opening; (b) involuntary jaw movements; (c)jaw function disabilities), which accompanied by increased electromyographic activity. Clinically, manifestations of lateral pterygoid myospasm which are more difficult to be observed, may be quite different,^[25],[26] so that the diagnosis is very hard to make for junior TMJ doctors. In addition, although electromyography can be used as a more objective index for the diagnosis of lateral pterygoid myospasm, the clinical application of electromyographic detection is also easily to be limited. The limitation is due principally to the deep anatomic location of LPM and its surrounding important nerves and blood vessels (e.g., pterygoid plexus) in cranio-maxillo-facial region. The necessity of local anesthesia for electromyographic electrode is invasive; it is easy to damage local vital tissues and lead to local infection, which will bring about unnecessary harm to the patients and aggravate their pain. Owing to the lack of knowledge of diagnostic basis of lateral pterygoid myospasm, finding out a new strategy has become particularly critical. Because of the advantages of non-invasion and non-radiation, MRI has been increasingly performed in clinical evaluation of skeletal muscle in recent years, for example, the measurement of muscular volume,^[29] the observation of muscular morphology,^[14],[30] and the recognition signal intensity change in T1 and T2 weighted imaging.^[31] Nevertheless, it is challenging for conventional MRI to detect subtle muscular changes.

Texture feature algorithms is a kind of radiological method that is to analysis and quantify the local properties, changeable regularities and distribution characteristics of grey scales of images. Not only does it support an omnibearing, objective, stable and noninvasive way to describe the pathological tissue without relying on the experience and subjective judgements of imaging doctors, it can also capture the elusive changes of tissue heterogeneity that can hardly be noted by the human visual system.^[32]

Texture contrast, defined as “what the values of metric matrix are distributed, and how much the local variations in image are”, reflects the clarity of image and the depth of textural groove; the deeper the groove pattern, the greater the texture contrast, the clearer the image effect.^[33] Through this current study, it is found that the contrast value of the healthy side was significantly larger than that of the affected side. The reason may be that the spasm of LPM causes involuntary contraction of the diseased muscle, resulting in muscular edema; in the edematous state, the groove will become shallow and the muscle texture will become blurred. Auto-correlation is also named as “Homogeneity,” which represents the linear dependency of grey levels of neighboring pixels; the autocorrelation is large as the values of matrix elements are uniform and equivalent.^[33] Opposite to the texture contrast, the weight of auto-correlation deceases along with the distance between the matrix element value and the diagonal; on the basis of the local homogeneity, the value of heterogeneous image is lower and that of homogeneous image is higher.^[34] In our study, the increased autocorrelation value was identified in the affected side, which suggested that the spasm of LPM emerged increased local gray level variation in MR T1 images. The increased autocorrelation value maybe connect with local homogeneous intensity, which may be influenced by ischemic area formed by the accumulation of metabolic waste resulting from intramuscular capillaries with long-term spasmodic contraction. The superficial texture discrepancies of strained LPMs chiefly tended to be the same, demonstrating a relatively less dissimilarity. The rest texture indices did not show the statistical significance between healthy and affected side, which suggested these texture features could not elucidate the lateral pterygoid myospasm pathogenesis probably because the sample capacity is too small.

In addition, in this study, we used GLCM, a popular second order texture analysis method to detect the relationship of the selected two points (usually two neighboring pixels) in different magnitude distance, and direction, which can quantitatively characterize the spatial distribution of pixels for the original image and extract the texture features from the gray information.^[34],[35] Nonetheless, the third and even higher order texture analyses methods (e.g., local binary patterns, histogram analysis, and gray-level run-length matrix) containing much more amount of parameters (e.g., dissimilarity, energy, maximum probability, color moment [first order-mean, second order-variance, and third order-skewness], color space, hue, saturation) have more potential to promote the diagnostic precision on lateral pterygoid myospasm.

Conclusion

In conclusion, up to now, our study reports the texture contrast and auto-correlation values are possible to be considered as effective variables for the diagnosis of spasm of for the first time; but further studies with regard to larger sample size, more advanced textural analytical techniques, more comprehensive scanning sequences with higher resolution MRI should be investigated to provide the direct imaging evidence as well as explain the mechanism for the variant status of lateral pterygoid myospasm.

Acknowledgments

The deepest gratitude goes first and foremost to Prof. Gong for his constant guidance and encouragement in all aspects. Second, the cordial appreciation is for Dr. Li who provided language help, writing assistance, and proof reading of this article. Last but not least, thanks a lot to Mr. Tao Zhang from Xinjiang Operation 3D Intelligence and Technology Co., Ltd, for his lecturing on about relevant surveying and mapping software.

Financial support and sponsorship

This study was supported by grants from Tianshan Innovation Team of Xinjiang Uygur Autonomous Region (No. 202110755; period of validity: Juy. 2021-Dec. 2023); and National Natural Science Foundation of China (No. 81760191; period of validity: Jan. 2018-Dec. 2021).

Conflicts of interest

Zhongcheng Gong is an Associate Editor of the journal. The article was subject to the journal's standard procedures, with peer review handled independently of this editor and his research groups.

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