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Shear Wave Elastography in the Evaluation of Temporomandibular Joint Disorders
ARTICLE IN PRESS Ultrasound in Med. & Biol., Vol. 00, No. 00, pp. 19, 2019 Copyright © 2019 World Federation for Ultrasound in Medicine & Biology. All rights reserved. Printed in the USA. All rights reserved. 0301-5629/$ - see front matter
https://doi.org/10.1016/j.ultrasmedbio.2019.09.014
Original Contribution SHEAR WAVE ELASTOGRAPHY IN THE EVALUATION OF TEMPOROMANDIBULAR JOINT DISORDERS AGEDPº T UKASZ
PALUCH,* PAULINA MAJ,y PIOTR PIETRUSKI,z MICHAº KORBA,x and BARTºOMIEJ H. NOSZCZYKzTAGEDEN
* Department of Radiology, Gruca Orthopedic and Trauma Teaching Hospital, Center of Postgraduate Medical Education, Otwock, Poland; y Department of Head and Neck Surgery, Military Institute of Medicine, Warsaw, Poland; z Department of Plastic Surgery, Or»owski Hospital, Center of Postgraduate Medical Education, Warsaw, Poland; and x Department of Cranio-Maxillofacial Surgery, Oral Surgery and Implantology, Medical University of Warsaw, Poland (Received 3 April 2019; revised 16 September 2019; in final from 18 September 2019)
Abstract—We aimed at verifying the usefulness of shear wave elastography in determining the temporomandibular disc stiffness in patients with a temporomandibular disorders (TMDs). The study included 37 patients with confirmed TMDs and 208 healthy volunteers. Patients presented with significantly greater stiffness of the intermediate zone of the disc (region of interest [ROI] 1) and significantly lower stiffness of its anteriorly displaced portion (ROI 3). A receiver operating characteristics analysis indicated that a decrease in the stiffness in ROI 3 less than 8.667 KPa provided 100% sensitivity, 97.3% specificity, 100% positive predictive value (PPV) and 99.5% negative predictive value (NPV) in distinguishing between patients with TMDs and without. Whereas an increase in ROI 1 stiffness to at least 54.33 KPa provided high specificity and NPV, both the sensitivity and the PPV of this predictor equaled zero. Findings suggest that a decrease in anteriorly dislocated disc stiffness less than 8.667 kPa can accurately identify patients with TMDs. (E-mail: [email protected]) © 2019 World Federation for Ultrasound in Medicine & Biology. All rights reserved. Key Words: Shear wave elastography, Temporomandibular joint, Temporomandibular disc elasticity, Temporomandibular disc displacement, Temporomandibular disorder.
has not been given due attention so far. Histologic structure of the disc shows substantial heterogeneity (Stankovic et al. 2013) between its thin intermediate zone and its thicker edges (Young 2015). In this conditions disc displacement contributes to the uneven distribution of forces that probably affect disc biomechanics (Abe et al. 2013). Persistent strains contribute to disc degeneration, which influences tissue stiffness (Iwasaki et al. 2017). Changes of disc stiffness were already found to be associated with TMD development in rats (Wang et al. 2014) and considered as a potential diagnostic tool (Yildrim et al. 2011). The stiffness or elasticity of tissues can be accurately determined using shear wave elastography (SWE). During SWE the particles that oscillate in tissue perpendicularly to the acoustic wave delivered by a transducer propagate as shear waves that are detected and measured. Based on the shear wave velocity within the examined tissue, its shear modulus can be calculated (Taljanovic et al. 2017). This parameter, as expressed in kilopascals (kPa), is a measure of tissue elasticity. The velocity of the shear wave within tissues of a greater
INTRODUCTION A temporomandibular joint (TMJ) can undergo degenerative processes that result in the development of temporomandibular disorders (TMDs). In most cases, TMDs are associated with the anterior dislocation of the articular disc of the TMJs. The development of TMDs is postulated to be a consequence of micro-injuries in the posterior capsule of a TMJ and of the retrodiscal tissue. Resulting predominance of muscular forces acting on the anterior part of the disc eventually lead to disc displacement (Butts et al. 2017). Magnetic resonance imaging (MRI) is currently considered a primary choice for TMD diagnoses (Larheim 2018), but none of the commonly used diagnostic modalities can be acknowledged as a gold standard (Strøm et al. 2013). However, some features of TMJ construction allow for searching for new solutions, which Address correspondence to: Bart»omiej H. Noszczyk, Department of Plastic Surgery, Orlowski Memorial Hospital, Center of Postgraduate Medical Education, Czerniakowska 231, 00-416 Warsaw, Poland. E-mail: [email protected]
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density is faster, and they are characterized by higher shear modulus values than more elastic ones (Taljanovic et al. 2017). SWE is generally considered to be objective, with the result not being investigator dependent (Vachutka et al. 2018). We hypothesized that the articular discs in patients with TMDs might gradually lose their elasticity, and this parameter, as determined by means of SWE, could serve as a marker of pathologic processes in TMJs. Therefore, the aim of this study was to verify the usefulness and diagnostic accuracy of SWE in determining the TMJ disc stiffness in patients with TMDs with anterior displacement. MATERIALS AND METHODS Ethics All procedures were conducted in accordance with the 1975 Declaration of Helsinki. The protocol of the study was approved by the University Bioethics Committee (decision no. 3/PB/2018) and written informed consent was sought from all the participants. Participants The study, conducted at the department of plastic surgery of a tertiary university hospital, included patients who were referred for radiologic evaluation because of a suspected TMD and, based on an MRI, were eventually diagnosed with anterior disc displacement. The inclusion criteria for this group were MRI symptoms of disk displacement (Orsini et al. 1998). The exclusion criteria were facial pain of different etiology and a recent history of craniofacial injuries. The control group was composed of asymptomatic volunteers who were referred to the department of plastic surgery for aesthetic procedures. All participants were asked to complete a version of the Diagnostic Criteria for Temporomandibular Disorders questionnaire (Osiewicz et al. 2018) and underwent clinical examination conducted by a maxillofacial surgeon with 5 y experience in the evaluation of TMJ pathologic conditions, to ultimately confirm (TMD group) or exclude (control group) the presence of TMDs. Shear wave elastography All participants of the study were subjected to a bilateral ultrasonography and SWE of the TMJ conducted by a radiologist with more than 5 y experience, blinded to the results of the MRI and clinical diagnosis. The ultrasonographic evaluation was carried out with a Toshiba iAplio 900 ultrasonograph with a 518 MHz transducer (Canon Medical Systems Europe, Zoetermeer, Netherlands). During the examination, the patients remained in the supine position, with their head stabilized and mouth maximally open. For the measurements,
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Fig. 1. The position of the transducer. Regions of interest (ROIs) are placed within the intermediate part of the disc (ROI 1); its displaced, anterior portion (ROI 3); and a halfway area between these points (ROI 2).
the transducer was positioned horizontally (Fig. 1). The distance between the TMJ capsule and condylar head (i.e., joint space width) was measured ultrasonographically (Fig. 2), followed by an SWE of the articular disc. The regions of interest (ROIs) with a diameter of 1 mm were placed within the intermediate part of the disc (ROI 1); its displaced, anterior portion (ROI 3); and a halfway area between these points (ROI 2) (Fig. 1). Each elastographic measurement was repeated three times at 5 min intervals, and the mean value from these three measurements was considered during the statistical analysis. In the final stage of the study, we invited an additional experienced radiologist blinded to the results of first evaluation to help us assess the inter-rater and intrarater reliability of the obtained results among selected volunteers from the control group. Statistical analysis The normal distribution of continuous variables was verified using the Shapiro-Wilk test. The statistical characteristics of the continuous variables were presented as arithmetical means, standard deviations, medians and ranges and the characteristics of the qualitative variables as numbers and percentages. The relationship between the stiffness of the intermediate and anteriorly displaced portions of the disc was analyzed based on the mean values of the ROI 1/ROI 3 stiffness ratios for the TMD group and the controls. The relationship between the stiffness of the intermediate portions in patients with TMDs and without (norm) was determined based on the mean values of the ROI 1TMD/ROI 1norm ratio, and the relationship between the stiffness of the displaced portions of the disc based on the mean values of the ROI 3norm/ROI 1TMD ratio. (Io facilitate a direct comparison of both ratios, they were constructed in such a way that the larger value was placed in the numerator and the smaller value in the denominator, regardless of the patient group it referred to.) The statistical significance of the between-group differences in the values of continuous variables was verified using the Mann-Whitney
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Fig. 2. The distance between the temporomandibular joint capsule and condylar head on the B-mode image. Extra-articular portion of the disc is turned to the left and indicated by arrow.
U test and the statistical significance of the betweengroup differences in the distributions of discrete variables using Pearson’s x2 and Fisher’s exact tests. The power and direction of the relationships between the pairs of continuous variables were determined based on the Spearman rank correlation coefficients (r). The diagnostic accuracy of the analyzed elastographic parameters in distinguishing between patients with a TMD and without was determined on a receiver operating characteristic (ROC) analysis. For each analyzed predictor (a variable distinguishing significantly between the TMD group and the controls), its sensitivity, specificity and positive and negative predictive values (PPV and NPV, respectively) were calculated, along with the area under the ROC curve (AUC) with its 95% confidence interval (CI). The roles of the patients’ age, sex and the TMD as independent determinants of the elastographic parameters were analyzed using a covariance analysis based on the values of the F statistics. Intra- and inter-rater reliability of the elastographic parameters was estimated based on intraclass correlation coefficients (ICCs) calculated for three measurements taken by two independent operators in 16 patients from the control group. All the calculations were carried out using the Statistica 10 package (StatSoft Inc., Tulsa, OK, USA), with the threshold of statistical significance set at p 0.05. RESULTS Participants The analysis included the data from 245 participants, among them 188 women (76.7%) and 57 men
(23.3%). The age of the study participants ranged between 19 and 84 y (median 52, mean 51.7 § 11.3). Based on the results from the MRI, 37 patients (15.1%), including 22 women (59.5%) and 15 men (40.5%), were diagnosed with bilateral TMDs. The control group, composed of 208 volunteers without TMDs (84.9%), included 166 women (79.8%) and 42 men (20.2%). Between-group comparisons Patients from the TMD group presented with significantly greater stiffness of the articular disc in ROI 1 and significantly lower stiffness of the disc in ROI 3 (Fig. 3a) than the controls (Fig. 3b; Table 1). Moreover, the individuals with TMDs were significantly younger than the other study participants. No statistically significant between-group differences were found in the joint space size (Table 1). Correlation analysis No statistically significant correlations between the joint space size and articular disc stiffness were found in the entire study series or in patients with TMDs and without. Because the stiffness in ROI 1 and ROI 3 turned out to be a parameter that distinguished persons with TMDs and without, we also analyzed the correlations between these two variables in the TMD and control group. Although a strong significant positive correlation between both variables was found in the controls (r = 0.847, p < 0.001; Fig. 4), this relationship lacked any statistical significance in the TMD group (r = 0.110, p = 0.516; Fig. 5). A primary reason behind the lack of significant
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Fig. 3. (a) The temporomandibular joint (TMJ) of the patient with the displaced portion of the disc turned to the right. Points T1, T2 and T3 correspond to region of interest (ROI) 1, ROI 2 and ROI 3, respectively. (b). The TMJ of a healthy control with the displaced portion of the disc turned to the left. Points T1, T2 and T3 correspond to ROI 1, ROI 2 and ROI 3, respectively.
correlation in the TMD group seemed to be a decrease in the stiffness in ROI 3. This conclusion is based on the comparison of the mean stiffness ratios of ROI 1/ROI 3 for the TMD and control group (8.2 and 1.2, respectively), as well as on the comparison of the mean stiffness ratios of ROI 1TMD/ROI 1norm (1.4) and ROI 3norm/ROI 3TMD (4.9). Based on these values, the disproportion in the stiffness of the intermediate and displaced portion of the disc in the TMD group was nearly eight times greater than in the controls. Furthermore, the relative between-group
differences in the articular disc stiffness were markedly more evident for ROI 3 than for ROI 1. Age and sex as potential confounders A statistically significant inverse correlation was found between the age of all the study participants and the articular disc stiffness in ROI 1 (r = 0.216, p = 0.001), along with a significant positive correlation between age and disc stiffness in ROI 3 (r = 0.172, p = 0.007). Moreover, in the control group, the disc stiffness in all the
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Table 1. Comparison of the statistical characteristics of age, joint space size and articular disc stiffness in patients with TMDs and healthy controls Variable
Age (y) Weight (kg) Body height (cm) BMI (kg/m2) Articular space width (mm) Stiffness in ROI 1 (kPa) Stiffness in ROI 2 (kPa) Stiffness in ROI 3 (kPa)
TMD group (n = 37)
Controls (n = 208)
mean § SD
median (range)
mean § SD
median (range)
41.2 § 16.0 69.6 § 17.3 171.5 § 10.1 23.4 § 4.1 1.7 § 0.4 36.7 § 4.6 25.1 § 17.5 4.5 § 2.1
38.0 (19.074.0) 66.0 (44113) 167 (152189) 23.7 (15.836.1) 1.6 (0.82.6) 36.3 (28.047.0) 33.3 (2.749.3) 4.0 (1.712.3)
53.6 § 9.0 67.7 § 13.6 170.1 § 8.3 23.3 § 3.6 1.6 § 0.4 26.4 § 7.3 32.7 § 7.8 22.1 § 6.6
53.0 (36.084.0) 66.0 (45112) 170.5 (153198) 23.1 (15.635.7) 1.5 (1.02.5) 24.3 (15.054.3) 30.7 (20.759.7) 21.3 (11.754.7)
p
<0.001 0.529 0.430 0.890 0.424 <0.001 0.551 <0.001
BMI = body mass index; ROI = region of interest; SD = standard deviation; TMD = temporomandibular disorder.
examined ROIs turned out to be significantly greater in men than in women. In contrast, no statistically significant sex-specific differences in the elastographic parameters of the articular disc were identified in the TMD group. Therefore, we verified whether the TMD group and the controls differed significantly in terms of their sex distributions. Indeed, the proportion of men in the TMD group turned out to be significantly higher than among the controls (40.5% vs. 20.2%, p = 0.011). During the next stage, a covariance analysis with explanatory variables “Age”, “Male sex” and “TMD” was conducted in order to verify whether the age and sex of the study participants were independent determinants of
between-group differences in the elastographic parameters of the disc in ROI 1 and ROI 3. The presence of a TMD turned out to be the only independent determinant of articular joint stiffness in both ROI 1 and ROI 3 (F = 43.633, p < 0.001 for ROI 1 and F = 203.391, p < 0.001 for ROI 3). The analysis of covariance did not identify any independent effect for age (F = 0.022, p = 0.882 for ROI 1 and F = 1.300, p = 0.255 for ROI 3) or sex (F = 2.030, p = 0.155 for ROI 1 and F = 2.071, p = 0.151 for ROI 3) on the values of both elastographic parameters. In addition, no significant effects of age*sex interaction were identified (F = 1.568, p = 0.212 for ROI 1 and F = 0.919, p = 0.339 for ROI 3).
Fig. 4. Significant positive correlation (r = 0.847, p < 0.001) between the stiffness of region of interest (ROI) 1 and ROI 3 in the control group.
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Fig. 5. No correlation (r = 0.110, p = 0.516) between the stiffness of region of interest (ROI) 1 and ROI 3 in the temporomandibular disorder group.
ROC analysis The ROC analysis indicated that a decrease in the articular disc stiffness in ROI 3 less 8.667 KPa provided 100% sensitivity, 97.3% specificity, 100% PPV and 99.5% NPV in distinguishing between patients with TMDs and without (AUC = 0.999, 95% CI 0.9981.000) (Fig. 6; Table 2). Whereas an increase in articular disc stiffness in ROI 1 to at least 54.333 KPa provided high specificity and NPV (99.5% and 84.8%, respectively) in distinguishing between the TMD group and the controls, both sensitivity and PPV of this predictor equaled zero (AUC = 0.879 95% CI 0.8370.921) (Fig. 7; Table 2). Intra- and inter-rater reliability Intra-rater reliability of the elastographic measurements taken by both operators exceeded 0.9 (ICC = 0.924, 95% CI 0.8800.954 and ICC = 0.925, 95% CI 0.8830.955, respectively), whereas inter-rater reliability was greater than 0.95 (ICC = 0.970, 95% CI 0.9590.978). DISCUSSION In this study, patients with TMDs presented with less stiffness of the anteriorly displaced part of the disc and greater stiffness of its intermediate zone than the
controls. In the early stages of a TMD, collagen fibers of the articular disc are exposed to multiple strains, which can lead to tissue fatigue. Under specific conditions, this can eventually result in the loss of the disc’s integrity (Iwasaki et al. 2017) and elasticity (Yildirim et al. 2011). However, various parts of discs react in different ways. It was clearly indicated in a rat model of a TMD, where a decrease in compressive and relaxation moduli was found in anterior and posterior bands rather than in the intermediate part of the disc, suggesting that a re-modeling of the bands makes them softer, rather than harder (Wang et al. 2014). The evidence from other studies also suggests that the articular disc in TMD patients might undergo a proteolytic remodeling. One study reported that a TMD was associated with an overexpression of ADAM10 protease in the posterior bands of the disc, which resulted in an enhanced breakdown of the aggrecan-rich matrix (Loreto et al. 2016). In another study, the immunoreactivity of ADAMTS-4, a metalloproteinase responsible for proteoglycan degradation, was found in the anterior bands of the disc (Leonardi et al. 2015). A decrease in anterior band elasticity could therefore be specific for a TMD. However, a second possibility should also be taken into account. It cannot be ruled out that because of the presence of an effusion in the TMJs of our patients, an exudate in the disc capsule was visualized and examined
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Fig. 6. The receiver operative characteristic curve for the articular disc stiffness in region of interest 3 (displaced portion) less than 8.667 kPa as a factor distinguishing between patients with temporomandibular disorders and healthy controls.
rather than the disc itself. Therefore, greater exudation could be responsible for the greater flexibility in the anterior part of the capsule. Our patients with a TMD and the healthy controls did not differ significantly in terms of the joint space size. Moreover, no significant correlation was found between the joint space size and the stiffness of the articular disc in either the TMD patients or the controls. An assessment of the joint space size, likewise in our study, has recently been proposed as an alternative to the direct method where the medial part of the joint is obscured by skeletal components (Klatkiewicz et al. 2018). According to certain authors, the size of the TMJ space correlates to the volume of the exudate (Bas et al. 2011; Johnston et al. 2015). However, as reported in our present study, the joint space width does not correlate with articular disc stiffness. Therefore, this implies that our elastographic measurements actually
involved the disc tissue, rather than the exudate. The lack of correlation between the width of the disk and its stiffness seems to be consistent with the heterogeneity of disc construction, reported by Stankovic et al. (2013). We found that, unlike in healthy controls, no correlation between the elastographic parameters of the parts of the disc was identified in TMD patients (Fig. 5). As already mentioned, a normal temporomandibular disc has a heterogeneous histologic structure and anisotropic mechanical properties (Stankovic et al. 2013). This biomechanical heterogeneity is considered to be a physiologic phenomenon (Gutman et al. 2018). However, despite this heterogeneity, biomechanical patterns between the elastographic parameters of the intermediate and anterior part of the disc were correlated in the healthy controls participating in our study (Fig. 4). The situation is different in the case of a TMD when the disc
Table 2. Diagnostic accuracy of the articular disc stiffness in distinguishing between patients with TMDs and healthy controls Variable
Cut-off value
Sensitivity
Specificity
PPV
NPV
AUC
Stiffness in ROI 1 (kPa) Stiffness in ROI 3 (kPa)
54.333 <8.667
0.000 0.973
0.995 1.000
0.000 1.000
0.848 0.995
0.879 (0.8370.921) 0.999 (0.9981.000)
AUC = area under the curve; NPV = negative predictive value; PPV = positive predictive value; ROI = region of interest; TMD = temporomandibular disorder.
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Fig. 7. The receiver operative characteristic curve for the articular disc stiffness in region of interest 1 (intermediate zone) of at least 54.333 KPa as a factor distinguishing between patients with temporomandibular disorders and healthy controls.
undergoes degenerative changes and deformations (Nickel et al. 2018), and its elasticity in various regions can change considerably (Roberts and Stocum 2018). The results of our study suggest that a change in the disc’s biomechanics in TMD patients is primarily a consequence of a lesser stiffness in its anteriorly displaced portion, rather than a result of a hardening in the intermediate zone as previously reported in rats (Wang et al. 2014). Furthermore, we found that regardless of the disc’s condition, older age predisposed the individual to a lesser stiffness of the disc in its intermediate part and a greater stiffness of its anterior portion. Previous results also indicated that the effect of aging on the disc’s stiffness is opposite to that as in the case of a chronic inflammation (Toure et al. 2005). The reasons behind this phenomenon are yet to be explained, but generally musculoskeletal disorders in elderly and younger populations may differ in terms of their course and diagnosis (Chang et al. 2017, 2018). We found that a decrease in the elastographically determined stiffness of the anteriorly displaced part of the TMJ disc provided high accuracy in the detection of a TMD. In turn, an increase in the stiffness of the intermediate part of the disc yielded high specificity and NPV, which implies that persons with stiffness less than 54.333
kPa are unlikely to present with TMD. However, the fact that such a high stiffness of the intermediate part of the disk was found in only one patient with TMD included in our series, and hence both sensitivity and PPV for this parameter equaled zero (Table 2), disqualifies it from the use as a standalone diagnostic measure. Considering the lack of generally accepted standards for ultrasonographic evaluations of TMJs (Klatkiewicz et al. 2018) and poor MRI availability in everyday practice, our observations could be of important clinical value. Wide clinical adoption of SWE is predictable in the coming years (Sigrist et al. 2017). Moreover, we believe that this modality will evolve and soon will be suitable for assessment of various stages of TMD development. It is known that viscoelatic properties of the discs change along with the content of proteoglycans (Tanaka et al. 2003), which, thanks to new SWE techniques, will be possible to study with increasing accuracy (Kijanka et al. 2019). Given the high intra- and inter-rater reliability of our measurements, such speculations might be justified. However, before the implementation of TMJ elastography to routine clinical practice, these findings need to be verified in larger groups of patients, because the relatively small sample size was, no doubt, a weakness in the present study. Another important limitation concerns the relevance of conclusions about the state
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of the entire articular disc based on the assessment of its part available for elastographic examination. The results of the SWE, just like the results of ultrasonographic disc evaluation, should be therefore interpreted with caution (Klatkiewicz et al. 2018). CONCLUSIONS To summarize, this study has provided the first evidence for the usefulness of SWE in the evaluation of patients with TMDs with anterior displacement. Our findings suggest that a decrease in the elastographically determined stiffness of the TMJ disc in its anteriorly displaced part to less than 8.667 kPa can accurately identify patients with a TMD, regardless of their age or sex. Acknowledgments—The authors would like to acknowledge Dr. Szymon Bruzewicz (SciencePro, http://www.sciencepro.co.kr) for his assistance in preparation of the manuscript. This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors. Conflict of interest disclosure—The authors declare no competing interests.
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https://doi.org/10.1016/j.ultrasmedbio.2019.09.014
Original Contribution SHEAR WAVE ELASTOGRAPHY IN THE EVALUATION OF TEMPOROMANDIBULAR JOINT DISORDERS AGEDPº T UKASZ
PALUCH,* PAULINA MAJ,y PIOTR PIETRUSKI,z MICHAº KORBA,x and BARTºOMIEJ H. NOSZCZYKzTAGEDEN
* Department of Radiology, Gruca Orthopedic and Trauma Teaching Hospital, Center of Postgraduate Medical Education, Otwock, Poland; y Department of Head and Neck Surgery, Military Institute of Medicine, Warsaw, Poland; z Department of Plastic Surgery, Or»owski Hospital, Center of Postgraduate Medical Education, Warsaw, Poland; and x Department of Cranio-Maxillofacial Surgery, Oral Surgery and Implantology, Medical University of Warsaw, Poland (Received 3 April 2019; revised 16 September 2019; in final from 18 September 2019)
Abstract—We aimed at verifying the usefulness of shear wave elastography in determining the temporomandibular disc stiffness in patients with a temporomandibular disorders (TMDs). The study included 37 patients with confirmed TMDs and 208 healthy volunteers. Patients presented with significantly greater stiffness of the intermediate zone of the disc (region of interest [ROI] 1) and significantly lower stiffness of its anteriorly displaced portion (ROI 3). A receiver operating characteristics analysis indicated that a decrease in the stiffness in ROI 3 less than 8.667 KPa provided 100% sensitivity, 97.3% specificity, 100% positive predictive value (PPV) and 99.5% negative predictive value (NPV) in distinguishing between patients with TMDs and without. Whereas an increase in ROI 1 stiffness to at least 54.33 KPa provided high specificity and NPV, both the sensitivity and the PPV of this predictor equaled zero. Findings suggest that a decrease in anteriorly dislocated disc stiffness less than 8.667 kPa can accurately identify patients with TMDs. (E-mail: [email protected]) © 2019 World Federation for Ultrasound in Medicine & Biology. All rights reserved. Key Words: Shear wave elastography, Temporomandibular joint, Temporomandibular disc elasticity, Temporomandibular disc displacement, Temporomandibular disorder.
has not been given due attention so far. Histologic structure of the disc shows substantial heterogeneity (Stankovic et al. 2013) between its thin intermediate zone and its thicker edges (Young 2015). In this conditions disc displacement contributes to the uneven distribution of forces that probably affect disc biomechanics (Abe et al. 2013). Persistent strains contribute to disc degeneration, which influences tissue stiffness (Iwasaki et al. 2017). Changes of disc stiffness were already found to be associated with TMD development in rats (Wang et al. 2014) and considered as a potential diagnostic tool (Yildrim et al. 2011). The stiffness or elasticity of tissues can be accurately determined using shear wave elastography (SWE). During SWE the particles that oscillate in tissue perpendicularly to the acoustic wave delivered by a transducer propagate as shear waves that are detected and measured. Based on the shear wave velocity within the examined tissue, its shear modulus can be calculated (Taljanovic et al. 2017). This parameter, as expressed in kilopascals (kPa), is a measure of tissue elasticity. The velocity of the shear wave within tissues of a greater
INTRODUCTION A temporomandibular joint (TMJ) can undergo degenerative processes that result in the development of temporomandibular disorders (TMDs). In most cases, TMDs are associated with the anterior dislocation of the articular disc of the TMJs. The development of TMDs is postulated to be a consequence of micro-injuries in the posterior capsule of a TMJ and of the retrodiscal tissue. Resulting predominance of muscular forces acting on the anterior part of the disc eventually lead to disc displacement (Butts et al. 2017). Magnetic resonance imaging (MRI) is currently considered a primary choice for TMD diagnoses (Larheim 2018), but none of the commonly used diagnostic modalities can be acknowledged as a gold standard (Strøm et al. 2013). However, some features of TMJ construction allow for searching for new solutions, which Address correspondence to: Bart»omiej H. Noszczyk, Department of Plastic Surgery, Orlowski Memorial Hospital, Center of Postgraduate Medical Education, Czerniakowska 231, 00-416 Warsaw, Poland. E-mail: [email protected]
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density is faster, and they are characterized by higher shear modulus values than more elastic ones (Taljanovic et al. 2017). SWE is generally considered to be objective, with the result not being investigator dependent (Vachutka et al. 2018). We hypothesized that the articular discs in patients with TMDs might gradually lose their elasticity, and this parameter, as determined by means of SWE, could serve as a marker of pathologic processes in TMJs. Therefore, the aim of this study was to verify the usefulness and diagnostic accuracy of SWE in determining the TMJ disc stiffness in patients with TMDs with anterior displacement. MATERIALS AND METHODS Ethics All procedures were conducted in accordance with the 1975 Declaration of Helsinki. The protocol of the study was approved by the University Bioethics Committee (decision no. 3/PB/2018) and written informed consent was sought from all the participants. Participants The study, conducted at the department of plastic surgery of a tertiary university hospital, included patients who were referred for radiologic evaluation because of a suspected TMD and, based on an MRI, were eventually diagnosed with anterior disc displacement. The inclusion criteria for this group were MRI symptoms of disk displacement (Orsini et al. 1998). The exclusion criteria were facial pain of different etiology and a recent history of craniofacial injuries. The control group was composed of asymptomatic volunteers who were referred to the department of plastic surgery for aesthetic procedures. All participants were asked to complete a version of the Diagnostic Criteria for Temporomandibular Disorders questionnaire (Osiewicz et al. 2018) and underwent clinical examination conducted by a maxillofacial surgeon with 5 y experience in the evaluation of TMJ pathologic conditions, to ultimately confirm (TMD group) or exclude (control group) the presence of TMDs. Shear wave elastography All participants of the study were subjected to a bilateral ultrasonography and SWE of the TMJ conducted by a radiologist with more than 5 y experience, blinded to the results of the MRI and clinical diagnosis. The ultrasonographic evaluation was carried out with a Toshiba iAplio 900 ultrasonograph with a 518 MHz transducer (Canon Medical Systems Europe, Zoetermeer, Netherlands). During the examination, the patients remained in the supine position, with their head stabilized and mouth maximally open. For the measurements,
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Fig. 1. The position of the transducer. Regions of interest (ROIs) are placed within the intermediate part of the disc (ROI 1); its displaced, anterior portion (ROI 3); and a halfway area between these points (ROI 2).
the transducer was positioned horizontally (Fig. 1). The distance between the TMJ capsule and condylar head (i.e., joint space width) was measured ultrasonographically (Fig. 2), followed by an SWE of the articular disc. The regions of interest (ROIs) with a diameter of 1 mm were placed within the intermediate part of the disc (ROI 1); its displaced, anterior portion (ROI 3); and a halfway area between these points (ROI 2) (Fig. 1). Each elastographic measurement was repeated three times at 5 min intervals, and the mean value from these three measurements was considered during the statistical analysis. In the final stage of the study, we invited an additional experienced radiologist blinded to the results of first evaluation to help us assess the inter-rater and intrarater reliability of the obtained results among selected volunteers from the control group. Statistical analysis The normal distribution of continuous variables was verified using the Shapiro-Wilk test. The statistical characteristics of the continuous variables were presented as arithmetical means, standard deviations, medians and ranges and the characteristics of the qualitative variables as numbers and percentages. The relationship between the stiffness of the intermediate and anteriorly displaced portions of the disc was analyzed based on the mean values of the ROI 1/ROI 3 stiffness ratios for the TMD group and the controls. The relationship between the stiffness of the intermediate portions in patients with TMDs and without (norm) was determined based on the mean values of the ROI 1TMD/ROI 1norm ratio, and the relationship between the stiffness of the displaced portions of the disc based on the mean values of the ROI 3norm/ROI 1TMD ratio. (Io facilitate a direct comparison of both ratios, they were constructed in such a way that the larger value was placed in the numerator and the smaller value in the denominator, regardless of the patient group it referred to.) The statistical significance of the between-group differences in the values of continuous variables was verified using the Mann-Whitney
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Fig. 2. The distance between the temporomandibular joint capsule and condylar head on the B-mode image. Extra-articular portion of the disc is turned to the left and indicated by arrow.
U test and the statistical significance of the betweengroup differences in the distributions of discrete variables using Pearson’s x2 and Fisher’s exact tests. The power and direction of the relationships between the pairs of continuous variables were determined based on the Spearman rank correlation coefficients (r). The diagnostic accuracy of the analyzed elastographic parameters in distinguishing between patients with a TMD and without was determined on a receiver operating characteristic (ROC) analysis. For each analyzed predictor (a variable distinguishing significantly between the TMD group and the controls), its sensitivity, specificity and positive and negative predictive values (PPV and NPV, respectively) were calculated, along with the area under the ROC curve (AUC) with its 95% confidence interval (CI). The roles of the patients’ age, sex and the TMD as independent determinants of the elastographic parameters were analyzed using a covariance analysis based on the values of the F statistics. Intra- and inter-rater reliability of the elastographic parameters was estimated based on intraclass correlation coefficients (ICCs) calculated for three measurements taken by two independent operators in 16 patients from the control group. All the calculations were carried out using the Statistica 10 package (StatSoft Inc., Tulsa, OK, USA), with the threshold of statistical significance set at p 0.05. RESULTS Participants The analysis included the data from 245 participants, among them 188 women (76.7%) and 57 men
(23.3%). The age of the study participants ranged between 19 and 84 y (median 52, mean 51.7 § 11.3). Based on the results from the MRI, 37 patients (15.1%), including 22 women (59.5%) and 15 men (40.5%), were diagnosed with bilateral TMDs. The control group, composed of 208 volunteers without TMDs (84.9%), included 166 women (79.8%) and 42 men (20.2%). Between-group comparisons Patients from the TMD group presented with significantly greater stiffness of the articular disc in ROI 1 and significantly lower stiffness of the disc in ROI 3 (Fig. 3a) than the controls (Fig. 3b; Table 1). Moreover, the individuals with TMDs were significantly younger than the other study participants. No statistically significant between-group differences were found in the joint space size (Table 1). Correlation analysis No statistically significant correlations between the joint space size and articular disc stiffness were found in the entire study series or in patients with TMDs and without. Because the stiffness in ROI 1 and ROI 3 turned out to be a parameter that distinguished persons with TMDs and without, we also analyzed the correlations between these two variables in the TMD and control group. Although a strong significant positive correlation between both variables was found in the controls (r = 0.847, p < 0.001; Fig. 4), this relationship lacked any statistical significance in the TMD group (r = 0.110, p = 0.516; Fig. 5). A primary reason behind the lack of significant
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Fig. 3. (a) The temporomandibular joint (TMJ) of the patient with the displaced portion of the disc turned to the right. Points T1, T2 and T3 correspond to region of interest (ROI) 1, ROI 2 and ROI 3, respectively. (b). The TMJ of a healthy control with the displaced portion of the disc turned to the left. Points T1, T2 and T3 correspond to ROI 1, ROI 2 and ROI 3, respectively.
correlation in the TMD group seemed to be a decrease in the stiffness in ROI 3. This conclusion is based on the comparison of the mean stiffness ratios of ROI 1/ROI 3 for the TMD and control group (8.2 and 1.2, respectively), as well as on the comparison of the mean stiffness ratios of ROI 1TMD/ROI 1norm (1.4) and ROI 3norm/ROI 3TMD (4.9). Based on these values, the disproportion in the stiffness of the intermediate and displaced portion of the disc in the TMD group was nearly eight times greater than in the controls. Furthermore, the relative between-group
differences in the articular disc stiffness were markedly more evident for ROI 3 than for ROI 1. Age and sex as potential confounders A statistically significant inverse correlation was found between the age of all the study participants and the articular disc stiffness in ROI 1 (r = 0.216, p = 0.001), along with a significant positive correlation between age and disc stiffness in ROI 3 (r = 0.172, p = 0.007). Moreover, in the control group, the disc stiffness in all the
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Table 1. Comparison of the statistical characteristics of age, joint space size and articular disc stiffness in patients with TMDs and healthy controls Variable
Age (y) Weight (kg) Body height (cm) BMI (kg/m2) Articular space width (mm) Stiffness in ROI 1 (kPa) Stiffness in ROI 2 (kPa) Stiffness in ROI 3 (kPa)
TMD group (n = 37)
Controls (n = 208)
mean § SD
median (range)
mean § SD
median (range)
41.2 § 16.0 69.6 § 17.3 171.5 § 10.1 23.4 § 4.1 1.7 § 0.4 36.7 § 4.6 25.1 § 17.5 4.5 § 2.1
38.0 (19.074.0) 66.0 (44113) 167 (152189) 23.7 (15.836.1) 1.6 (0.82.6) 36.3 (28.047.0) 33.3 (2.749.3) 4.0 (1.712.3)
53.6 § 9.0 67.7 § 13.6 170.1 § 8.3 23.3 § 3.6 1.6 § 0.4 26.4 § 7.3 32.7 § 7.8 22.1 § 6.6
53.0 (36.084.0) 66.0 (45112) 170.5 (153198) 23.1 (15.635.7) 1.5 (1.02.5) 24.3 (15.054.3) 30.7 (20.759.7) 21.3 (11.754.7)
p
<0.001 0.529 0.430 0.890 0.424 <0.001 0.551 <0.001
BMI = body mass index; ROI = region of interest; SD = standard deviation; TMD = temporomandibular disorder.
examined ROIs turned out to be significantly greater in men than in women. In contrast, no statistically significant sex-specific differences in the elastographic parameters of the articular disc were identified in the TMD group. Therefore, we verified whether the TMD group and the controls differed significantly in terms of their sex distributions. Indeed, the proportion of men in the TMD group turned out to be significantly higher than among the controls (40.5% vs. 20.2%, p = 0.011). During the next stage, a covariance analysis with explanatory variables “Age”, “Male sex” and “TMD” was conducted in order to verify whether the age and sex of the study participants were independent determinants of
between-group differences in the elastographic parameters of the disc in ROI 1 and ROI 3. The presence of a TMD turned out to be the only independent determinant of articular joint stiffness in both ROI 1 and ROI 3 (F = 43.633, p < 0.001 for ROI 1 and F = 203.391, p < 0.001 for ROI 3). The analysis of covariance did not identify any independent effect for age (F = 0.022, p = 0.882 for ROI 1 and F = 1.300, p = 0.255 for ROI 3) or sex (F = 2.030, p = 0.155 for ROI 1 and F = 2.071, p = 0.151 for ROI 3) on the values of both elastographic parameters. In addition, no significant effects of age*sex interaction were identified (F = 1.568, p = 0.212 for ROI 1 and F = 0.919, p = 0.339 for ROI 3).
Fig. 4. Significant positive correlation (r = 0.847, p < 0.001) between the stiffness of region of interest (ROI) 1 and ROI 3 in the control group.
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Fig. 5. No correlation (r = 0.110, p = 0.516) between the stiffness of region of interest (ROI) 1 and ROI 3 in the temporomandibular disorder group.
ROC analysis The ROC analysis indicated that a decrease in the articular disc stiffness in ROI 3 less 8.667 KPa provided 100% sensitivity, 97.3% specificity, 100% PPV and 99.5% NPV in distinguishing between patients with TMDs and without (AUC = 0.999, 95% CI 0.9981.000) (Fig. 6; Table 2). Whereas an increase in articular disc stiffness in ROI 1 to at least 54.333 KPa provided high specificity and NPV (99.5% and 84.8%, respectively) in distinguishing between the TMD group and the controls, both sensitivity and PPV of this predictor equaled zero (AUC = 0.879 95% CI 0.8370.921) (Fig. 7; Table 2). Intra- and inter-rater reliability Intra-rater reliability of the elastographic measurements taken by both operators exceeded 0.9 (ICC = 0.924, 95% CI 0.8800.954 and ICC = 0.925, 95% CI 0.8830.955, respectively), whereas inter-rater reliability was greater than 0.95 (ICC = 0.970, 95% CI 0.9590.978). DISCUSSION In this study, patients with TMDs presented with less stiffness of the anteriorly displaced part of the disc and greater stiffness of its intermediate zone than the
controls. In the early stages of a TMD, collagen fibers of the articular disc are exposed to multiple strains, which can lead to tissue fatigue. Under specific conditions, this can eventually result in the loss of the disc’s integrity (Iwasaki et al. 2017) and elasticity (Yildirim et al. 2011). However, various parts of discs react in different ways. It was clearly indicated in a rat model of a TMD, where a decrease in compressive and relaxation moduli was found in anterior and posterior bands rather than in the intermediate part of the disc, suggesting that a re-modeling of the bands makes them softer, rather than harder (Wang et al. 2014). The evidence from other studies also suggests that the articular disc in TMD patients might undergo a proteolytic remodeling. One study reported that a TMD was associated with an overexpression of ADAM10 protease in the posterior bands of the disc, which resulted in an enhanced breakdown of the aggrecan-rich matrix (Loreto et al. 2016). In another study, the immunoreactivity of ADAMTS-4, a metalloproteinase responsible for proteoglycan degradation, was found in the anterior bands of the disc (Leonardi et al. 2015). A decrease in anterior band elasticity could therefore be specific for a TMD. However, a second possibility should also be taken into account. It cannot be ruled out that because of the presence of an effusion in the TMJs of our patients, an exudate in the disc capsule was visualized and examined
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Fig. 6. The receiver operative characteristic curve for the articular disc stiffness in region of interest 3 (displaced portion) less than 8.667 kPa as a factor distinguishing between patients with temporomandibular disorders and healthy controls.
rather than the disc itself. Therefore, greater exudation could be responsible for the greater flexibility in the anterior part of the capsule. Our patients with a TMD and the healthy controls did not differ significantly in terms of the joint space size. Moreover, no significant correlation was found between the joint space size and the stiffness of the articular disc in either the TMD patients or the controls. An assessment of the joint space size, likewise in our study, has recently been proposed as an alternative to the direct method where the medial part of the joint is obscured by skeletal components (Klatkiewicz et al. 2018). According to certain authors, the size of the TMJ space correlates to the volume of the exudate (Bas et al. 2011; Johnston et al. 2015). However, as reported in our present study, the joint space width does not correlate with articular disc stiffness. Therefore, this implies that our elastographic measurements actually
involved the disc tissue, rather than the exudate. The lack of correlation between the width of the disk and its stiffness seems to be consistent with the heterogeneity of disc construction, reported by Stankovic et al. (2013). We found that, unlike in healthy controls, no correlation between the elastographic parameters of the parts of the disc was identified in TMD patients (Fig. 5). As already mentioned, a normal temporomandibular disc has a heterogeneous histologic structure and anisotropic mechanical properties (Stankovic et al. 2013). This biomechanical heterogeneity is considered to be a physiologic phenomenon (Gutman et al. 2018). However, despite this heterogeneity, biomechanical patterns between the elastographic parameters of the intermediate and anterior part of the disc were correlated in the healthy controls participating in our study (Fig. 4). The situation is different in the case of a TMD when the disc
Table 2. Diagnostic accuracy of the articular disc stiffness in distinguishing between patients with TMDs and healthy controls Variable
Cut-off value
Sensitivity
Specificity
PPV
NPV
AUC
Stiffness in ROI 1 (kPa) Stiffness in ROI 3 (kPa)
54.333 <8.667
0.000 0.973
0.995 1.000
0.000 1.000
0.848 0.995
0.879 (0.8370.921) 0.999 (0.9981.000)
AUC = area under the curve; NPV = negative predictive value; PPV = positive predictive value; ROI = region of interest; TMD = temporomandibular disorder.
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Fig. 7. The receiver operative characteristic curve for the articular disc stiffness in region of interest 1 (intermediate zone) of at least 54.333 KPa as a factor distinguishing between patients with temporomandibular disorders and healthy controls.
undergoes degenerative changes and deformations (Nickel et al. 2018), and its elasticity in various regions can change considerably (Roberts and Stocum 2018). The results of our study suggest that a change in the disc’s biomechanics in TMD patients is primarily a consequence of a lesser stiffness in its anteriorly displaced portion, rather than a result of a hardening in the intermediate zone as previously reported in rats (Wang et al. 2014). Furthermore, we found that regardless of the disc’s condition, older age predisposed the individual to a lesser stiffness of the disc in its intermediate part and a greater stiffness of its anterior portion. Previous results also indicated that the effect of aging on the disc’s stiffness is opposite to that as in the case of a chronic inflammation (Toure et al. 2005). The reasons behind this phenomenon are yet to be explained, but generally musculoskeletal disorders in elderly and younger populations may differ in terms of their course and diagnosis (Chang et al. 2017, 2018). We found that a decrease in the elastographically determined stiffness of the anteriorly displaced part of the TMJ disc provided high accuracy in the detection of a TMD. In turn, an increase in the stiffness of the intermediate part of the disc yielded high specificity and NPV, which implies that persons with stiffness less than 54.333
kPa are unlikely to present with TMD. However, the fact that such a high stiffness of the intermediate part of the disk was found in only one patient with TMD included in our series, and hence both sensitivity and PPV for this parameter equaled zero (Table 2), disqualifies it from the use as a standalone diagnostic measure. Considering the lack of generally accepted standards for ultrasonographic evaluations of TMJs (Klatkiewicz et al. 2018) and poor MRI availability in everyday practice, our observations could be of important clinical value. Wide clinical adoption of SWE is predictable in the coming years (Sigrist et al. 2017). Moreover, we believe that this modality will evolve and soon will be suitable for assessment of various stages of TMD development. It is known that viscoelatic properties of the discs change along with the content of proteoglycans (Tanaka et al. 2003), which, thanks to new SWE techniques, will be possible to study with increasing accuracy (Kijanka et al. 2019). Given the high intra- and inter-rater reliability of our measurements, such speculations might be justified. However, before the implementation of TMJ elastography to routine clinical practice, these findings need to be verified in larger groups of patients, because the relatively small sample size was, no doubt, a weakness in the present study. Another important limitation concerns the relevance of conclusions about the state
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of the entire articular disc based on the assessment of its part available for elastographic examination. The results of the SWE, just like the results of ultrasonographic disc evaluation, should be therefore interpreted with caution (Klatkiewicz et al. 2018). CONCLUSIONS To summarize, this study has provided the first evidence for the usefulness of SWE in the evaluation of patients with TMDs with anterior displacement. Our findings suggest that a decrease in the elastographically determined stiffness of the TMJ disc in its anteriorly displaced part to less than 8.667 kPa can accurately identify patients with a TMD, regardless of their age or sex. Acknowledgments—The authors would like to acknowledge Dr. Szymon Bruzewicz (SciencePro, http://www.sciencepro.co.kr) for his assistance in preparation of the manuscript. This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors. Conflict of interest disclosure—The authors declare no competing interests.
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