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Advanced Ultrasound Screening for Temporomandibular Joint (TMJ) Internal Derangement

Advanced Ultrasound Screening for Temporomandibular Joint (TMJ) Internal Derangement Hindawi Radiology Research and Practice Volume 2020, Article ID 1809690, 10 pages https://doi.org/10.1155/2020/1809690 Research Article Advanced Ultrasound Screening for Temporomandibular Joint (TMJ) Internal Derangement 1 2 3 3 Saul N. Friedman , Miriam Grushka, Hussam K. Beituni, Madhu Rehman, 4 3 Hart B. Bressler , and Lawrence Friedman Division of Nuclear Medicine, Mallinckrodt Institute of Radiology, Washington University School of Medicine, Saint Louis, MO 63110, USA 974 Eglington Avenue West, Toronto, Ontario M6C 2C5, Canada Department of Medical Imaging, North York General, 4001 Leslie Street, Toronto, Ontario M2K 1E1, Canada Department of Family and Community Medicine, University of Toronto, Mount Sinai Hospital, 600 University Ave, Toronto, Ontario M5G 1X5, Canada Correspondence should be addressed to Saul N. Friedman; saul.friedman@gmail.com Received 25 December 2019; Accepted 17 February 2020; Published 4 May 2020 Academic Editor: Henrique M. Lederman Copyright © 2020 Saul N. Friedman et al. ,is is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Purpose. To present an advanced ultrasound (US) technique and propose its use as a screening diagnostic tool for temporo- mandibular joint (TMJ) internal derangement. Materials and Methods. ,e technique is based on maintaining the US probe parallel to the articular disc, rather than traditional axial and coronal views, with the position described relative to a clock face. Validation was achieved by direct comparison with magnetic resonance imaging (MRI). A total of 61 patients, with age ranging from 13 to 67 years, were prescreened for TMJ pain and internal derangement, underwent US imaging for screening, and MRI evaluation for final diagnosis. Results. 29 of the 61 patients had disc pathology on MRI. US screening produced no false positive results and only 6 false negative results, corresponding to a sensitivity of 79% and specificity of 100%. Half of the false negative cases involved disc pathology with a medial component to the disc displacement. Conclusion. US is both a sensitive and a specific screening tool for TMJ dysfunction when used by an appropriately trained operator, with the exception of medially displaced discs. If TMJ assessment is found to be abnormal, the patient should be referred for MRI, and any patient scheduled for surgery must have the diagnosis confirmed by MRI. If a component of medial disc displacement is suspected, MRI should be performed despite a normal screening US. examination, however, takes 20 to 45 minutes on average to 1. Introduction perform depending on the scanner and protocol, and pa- In the past, internal derangement of the temporomandibular tients have difficulty keeping still and having their mouths joint (TMJ) has been assessed with plain film radiographs as open for extended periods of time, especially if they are the initial investigation [1] followed by arthrography [2] and experiencing pain. In addition, the examination is costly and computed tomography (CT) [3]. More recently, magnetic access is still limited in many centres. Many patients also resonance imaging (MRI) [4–7] has provided a noninvasive experience claustrophobia and are unable to complete or accurate method of assessing the TMJ without associated even undergo the examination. radiation risks. Its advantages over previous methods in- Ultrasound is relatively inexpensive, is readily accessible, clude its ability to directly visualize the disc and accurately and can be performed in most outpatient facilities; studies determine the position of the disc with respect to the condyle take only an average of 10 to 15 minutes in total, and it is of the mandible and eminence of the temporal bone. ,e without any known risks. In addition, US provides the 2 Radiology Research and Practice opportunity to converse with patients and identify the exact 2.1. Ultrasound Technique Details. ,e patient can be in a locations of pain, while the probe can be used as a palpable sitting position or lying down on a stretcher. We prefer the tool for real-time identification of crepitus, clicking, motion, patients lying supine with the jaw tilted away from the side to and snapping sensations. ,e disadvantages of US remain be examined, as this position not only offers more stability the long learning curve and the fact that the test is operator for probe positioning but also allows for further patient dependent. ,ere is also the question of ultrasound being comfort. ,e joint is then palpated while we have the patient effectively used as a diagnostic tool [8–13], given the many open and close their mouth. Once the joint is located, the constraints that will be discussed. In particular, Katzberg probe is placed over the joint using a liberal amount of warm [12] questioned its validity stating that ultrasound images do gel. not appear to be anatomically correct, that tissues indicated Traditional ultrasound techniques have included posi- to be discs were not convincing, and that interpretation was tioning of the probe on the skin surface in the axial not blinded. He also believed that given the bone blockade (Figure 1(a)) and coronal (Figure 1(b)) planes [12, 13]. We barrier and inability of the ultrasound beam to bend around employ a method whereby the position of the probe can be curved narrow structures, ultrasound does not allow for compared to that of a clock face in a clockwise rotation. ,e adequate diagnosis. However, more recently, Katzberg and probe is angled appropriately parallel to the right disc in the colleagues have proposed the use of sagittal transoral US to sagittal plane initially at an angle 50–60 down from the evaluate the TMJ [14]. horizontal as measured from the anterior side of the probe or Additional and more recent works by numerous in- 5 o’clock in the closed-mouth position on the right vestigators provide strong support for the use of conven- (Figure 1(c)), followed by 0 angulation or 3 o’clock in the tional US techniques. For example, Li et al. [13] in 2012 semiopen position (Figure 1(d)), and finally an anterior calculated a sensitivity and specificity of 76% and 82% for angle of 50–60 up from the horizontal as measured from the disc displacement with reduction, respectively, and 79% and anterior side of the probe or 1 o’clock in the fully open- 91% without disc reduction, respectively. ,ey also stated mouth position on the right (Figure 1(e)). In a similar that ultrasound is acceptable as a rapid initial method to manner, these angles would correspond to 7 o’clock, 9 exclude some potential patients but recommended MRI if o’clock, and 11 o’clock positions, respectively, when in- treatment is necessary. In addition, they noted that the vestigating the left TMJ. Dynamic video clips of movement ability to diagnose lateral and posterior displacements by can be obtained by swivelling the probe or by keeping the ultrasound is not clear. More recently, Su et al. published a probe just off the horizontal, which varies from patient to meta-analysis in 2018 noting an overall sensitivity and patient. specificity of 75–81% and 73–80%, respectively, for disc ,e disc was considered normal in the static closed- displacement in the closed-mouth position and 65–74% and mouth position if the intermediate zone or centre of the 86–91%, respectively, for disc displacement in the open- hypoechoic disc was located between the anterosuperior mouth position [15]. aspect of the condyle and the posteroinferior aspect of the Katzberg [12] attempted to quantify the distribution of disc articular eminence. During movement, the disc was con- displacements in a prospective study of 76 volunteers and 102 sidered normal if the intermediate zone or centre of the disc patients studied with MRI. He noted 52% of abnormal joints maintained its central location to the condyle from the had anterior displacement, 27% of abnormal joints had closed-mouth to fully open-mouth positions. All other disc anteromedial displacement, 12% of abnormal joints had medial locations were considered to exhibit either anterior or displacement, 34% of abnormal joints had anterolateral dis- posterior displacement. placement, and 4% of abnormal joints had lateral displacement. He also stated that anteromedially and medially displaced discs, 2.2. Imaging Equipment. Ultrasound images were obtained totalling 39%, would not be visualized by ultrasound. using a 15–7 MHz L15-7io hockey stick transducer (Philips iU22 Ultrasound System, Netherlands). ,e total US image acquisition time was approximately 10 minutes per patient. 1.1. Goal. Using knowledge of the normal US appearance and MRI was performed using T1 coronal and sagittal images dynamic motion of the articular disc, we present a new tech- in both open- and closed-mouth positions as well as gradient nique for visualization and assessment of the TMJ using ul- kinetic dynamic sagittal images (GE Signa HDxt 1.5T, trasound, where the probe is positioned parallel to the disc Milwaukee, USA) with the following parameters: coronal throughout movement; this technique differs from traditional T1-weighted images with repetition time (TR) = 405 ms and vertical and horizontal probe positioning, where the focus has echo time (TE) = 10 ms, sagittal proton-density-weighted been on obtaining true axial and coronal plains of imaging. MRI images with TR = 2025 ms and TE = 30 ms, and sagittal T2 - of the TMJ is used as the gold standard for technique validation. weighted kinematic dynamic images with TR = 100 ms and TE = 10 ms. ,e total acquisition time was approximately 2. Materials and Methods 30 minutes per patient. Institutional review board approval from North York General Ethics Committee was obtained, and verbal consent 2.3. Validation with Normal Volunteers. Normal anatomy was obtained from all patients and subjects prior to inclusion was first reviewed through the evaluation of both TMJs in 10 in the study. normal volunteers between the ages of 20 and 30 years. Radiology Research and Practice 3 (a) (b) (c) (d) (e) Figure 1: Position of the probe on the skin surface for traditional (a) transverse and (b) coronal scans. ,e probe position during routine interrogation of the TMJ is (c) angled parallel to the disc in the sagittal plane at 50–60 below the horizontal as measured from the anterior side of the probe or 5 o’clock position in the closed-mouth position on the right, (d) angled parallel to the disc or 3 o’clock position in the half-open-mouth position on the right, and (e) angled 50–60 above the horizontal as measured from the anterior side of the probe in the fully open-mouth or 1 o’clock position on the right. In a similar manner, these angles represent 7 o’clock, 9 o’clock, and 11 o’clock positions when investigating the TMJ on the left. 2.4. Assessment of Patient Pathology. Patients were pre- delay in patient care. ,e same senior MSK radiologist with screened for TMJ pain and internal derangement based on over 20 years of specialized US MSK training performed all the history and clinical exam by our TMJ pathology spe- US interpretations. To avoid recall bias, the US reader cialist (author MG) or our pain specialist with particular remained blinded to all MRI results performed by other experience in TMJ pathology (author HBB). Recommen- readers. In addition, in the situation where the US reader dations on the physical exam technique have been described also interpreted the MRI first, a period of 3-4 weeks was in detail elsewhere [16]. A total of 61 symptomatic patients waited after the MRI interpretation before interpreting the were recruited, of which 43 were male and 18 female with a associated US. mean age of 40 years and age range of 13 to 67 years. MR and ,e US screen was considered positive if displacement US imaging was obtained using the same equipment and was observed, regardless of the direction (anterior, posterior, protocol as above. All US images were acquired by the senior medial, or lateral) and regardless of whether it reduced or radiologist (author LF), who had over 20 years of specialized remained fixed. In cases where displacement was observed in US MSK experience. Contrast was not used for either MR or multiple directions (e.g., anteromedial), the displacement US imaging. MRI interpretations were performed by 4 ra- was labelled by the predominant direction of displacement. diologists, each with a minimum of 5 years of experience Pathology was then further subdivided into fixed displace- working in a practice, and typically completed first to avoid ment and recapture subgroups. Osteoarthritic changes and 4 Radiology Research and Practice Figure 2: Normal anatomy illustrating the condyle of the mandible, superior and inferior belly of the lateral pterygoid muscle, articular disc, articular eminence of the temporal bone, and articular fossa (glenoid fossa) of the temporal bone. evidence of inflammation as determined through increased closely applied cortical surface of the condyle and the blood flow were also evaluated but could only be performed eminence. Close attention to this relationship is critical in on US as MRI postcontrast imaging was not performed. separating a normal from an abnormal disc on both MRI and ultrasound interrogation. For a right-sided TMJ in the closed-mouth position in the sagittal plane, the anterior 3. Results angle of the normal disc is 50–60 down from the hori- 3.1. Normal TMJ. A diagram of basic anatomy is presented zontal. When midway between open- and closed-mouth in Figure 2 as a visual aid. ,e articular disc in the normal positions, the anterior angle is 0 to the horizontal, and in TMJ is a fibrous structure composed of a superficial band, a the fully-open-mouth position, it is 50–60 up from the slightly more thickened deep band, and a very thin inter- horizontal. ,e mirror image configuration is present in the mediate zone that is attached posteriorly to the temporal left-sided TMJ. bone through the bilaminar zone and anteriorly to the lateral pterygoid muscle superior belly. A lower synovial-lined joint space separates it from the head of the condyle, and a 3.2. Abnormal TMJ. Pathology for the 61 patients included noncommunicating upper joint separates it from the bony in the study as determined by MRI is summarized in glenoid fossa and the articular eminence of the temporal Table 1. ,e 29 patients positive for TMJ pathology cor- bone. respond to a prevalence of 47.5%. Fixed posterior dis- On MRI, the disc has a bowtie or saddle appearance. On placement was not observed. Of the 14 patients with fixed sonography, a normal disc usually appears as an inverted anterior displacement, 3 were noted to have a medial more hypoechoic c-shaped structure that straddles the component to the displacement. Lateral disc displacement hyperechoic cortex of the condyle, as seen in Figure 3. was not observed. However, the disc can also appear isoechoic to hyperechoic Ultrasound screening identified 23 of the 29 patients especially as it becomes less hydrated and more calcified with with pathology, corresponding to 6 false negatives. No false disease. positive results were obtained. ,is corresponds to a sen- During normal movement and disc translation, the disc sitivity of 79% and specificity of 100%; results are sum- maintains a constant relationship between the condyle marized in Table 2. ,e 6 false negative cases all head of the mandible and the eminence of the temporal corresponded to fixed anterior displacement and included bone. From the closed-mouth to the fully-open-mouth all 3 cases that were noted to contain a medial component of position, the thin intermediate zone should be between the displacement. Based on the calculated prevalence of 47.5%, Radiology Research and Practice 5 Figure 3: Normal ultrasound appearance of the articular disc in the sagittal plane, seen as an inverted hypoechoic c-shaped structure. Note that the disc maintains a constant central appearance with respect to the centre of the condyle, “c,” outlined by a central vertical line during the closed-mouth, half-open-mouth, and fully-open-mouth views. ,e anterior (“ant”) band and posterior band of the articular disc appear symmetrical in size with respect to the centre of the condyle. A focal annotated view was provided to aid visualization with the articular disc outlined with a dotted contour. the calculated positive predictive value is 100% and the fixed anterior dislocation, is demonstrated in Figure 5. While negative predictive value is 84%. the morphology of the disc usually remains normal with US and MRI of anterior disc displacement with recapture an anteriorly displaced disc that recaptures, it more often of the disc in the open-mouth position are demonstrated in appears morphologically abnormal with fixed anterior Figure 4. Note the normal MRI bowtie appearance in Figure dislocation, as noted in Figure 5. Posterior displacement 4(b). Corresponding pathology without recapture, labelled as is demonstrated in Figure 6. Bony deformity and bony 6 Radiology Research and Practice Table 1: A total of 29 of the 61 patients experiencing temporomandibular symptoms had pathology visible on magnetic resonance imaging (MRI), corresponding to a disease prevalence of 47.5%. Pathology is subdivided into anterior, posterior, and medial displacements and summarized here, with the number demonstrating the presence of recapture, osteoarthritic changes, and presence of inflammation (as determined from ultrasound imaging) noted. Pathological disc displacement Fixed Recapture present Total Anterior 14 14 28 Posterior 0 1 1 Medial 0 0 0 Lateral 0 0 0 Total 14 15 29 3 cases were further noted to have a medially displaced component. Table 2: Summary of results of the 61 patients prescreened for temporomandibular symptoms using ultrasound (US) and compared to the gold standard of magnetic resonance imaging (MRI). US results are split into true positive and true negative (concordant with MRI), and false positive and false negative (discordant with MRI), corresponding to a sensitivity of 79% and specificity of 100%. MRI screened positive MRI screened negative US screened positive 23 0 US screened negative 6 32 (a) (b) (c) (d) Figure 4: Images demonstrating anterior displacement of the disc in the sagittal plane in the (a) closed-mouth position with MR, (b) disc recapture in the open-mouth position with MR, (c) closed-mouth position with US, and (d) recapture in the open-mouth position with US. ,e disc retains normal morphology. A focal annotated view was provided to aid visualization with the articular disc outlined with a dotted contour; condyle � “c”; eminence � “e”; anterior � “ant.” Radiology Research and Practice 7 (a) (b) (c) (d) Figure 5: Images demonstrating a deformed disc with fixed anterior dislocation in the sagittal plane in the (a) closed-mouth position with MRI, (b) open-mouth position with MRI, (c) closed-mouth position with US, and (d) open-mouth position with US. A focal annotated view was provided to aid visualization with the articular disc outlined with a dotted contour; condyle � “c”; anterior � “ant”; left � “LT.” (a) (b) Figure 6: Continued. 8 Radiology Research and Practice (c) (d) Figure 6: Images demonstrating posterior displacement of the disc in the (a) closed-mouth position with MRI, (b) recapture in the open- mouth position with MRI, (c) closed-mouth position with US, and (d) recapture in the open-mouth position with US. A focal annotated view was provided to aid visualization with the articular disc outlined with a dotted contour; anterior � “ant”; condyle � “c”; left � “LT.” likely imaging prevalence. While the power of our study is osteophyte formation in osteoarthritis involving the condyle can be visualized on ultrasound, as demonstrated limited, we believe our results to be sufficient for the initial validation of US as a screening tool to help decide who in Figure 7. should proceed with additional MRI. We continue to screen patients with our US technique and have evaluated 4. Discussion more than 350 additional patients; however, lack of cor- We introduce an advanced technique for evaluating the responding MRI evaluation prevented their inclusion in temporomandibular joint through ultrasound imaging this study. by positioning the probe parallel to the articular disc Ethical management, requiring a definitive diagnosis for throughout dynamic motion. US was presented as a treatment to not be delayed, prevented US image acquisition screening tool for TMJ dysfunction due to its ubiquitous and interpretation prior to MRI evaluation. Potential bias was minimized by limiting the number of MRIs interpreted nature and relatively inexpensive cost. MRI was chosen as the gold standard for comparison due to its high level by the expert radiologist who interpreted the US studies, and keeping him ignorant of MRI results until assessment of the of specificity and sensitivity, as well as its role in current standard of practice. US images was completed. In cases where the MRI was read We have limited our description of articular disc pa- first by the same radiologist who read the subsequent US, the thology to anterior, posterior, medial, and lateral dislo- US interpretation was held for 3-4 weeks to minimize recall cation, based on the most prominent feature only. While bias. this creates labelling bias, this is unlikely to affect the Of the 6 false negative cases obtained using our tech- patient outcome as the primary role is screening and nique, all cases noted to involve medial disc displacement subsequent MRI studies were performed for further were included. ,is is likely due to the limited penetrance of characterization. Lateral displacement was not visualized US because of bone and other anatomy, restricting it to the superficial one-third of the disc. Others have also noted that in our study; however, this is not unexpected. Based on the 4% prevalence of lateral displacement by Katzberg et al. laterally or medially displaced discs are known to be in- adequately visualized and evaluated with present ultrasound [17], only a single case is expected within a group of 29, and random chance alone is enough to explain its absence. techniques [13]. However, medial and lateral displacements were generally Advantages of US over MRI identified during our study difficult to visualize on US and are likely underestimated include the ability to observe real-time motion, clicking based on US alone. Validation of lateral displacement on and crepitus, the ability to localize imaging to patient- US will require a much larger sample size given the relative directed regions of pain, and the ability to evaluate patients rarity. who are claustrophobic or have stents and implants that are Prescreening patients for TMJ symptoms inherently not MRI compatible. Doppler imaging enabled us to di- creates a selection bias, with our measured prevalence of agnose inflammation by the presence of abnormal blood flow that, while theoretically possible if contrast is used, is 47.5% grossly overestimating prevalence in the general population, but reflecting realistic clinical practice and the unlikely on MRI with standard practices. US is also able to Radiology Research and Practice 9 (a) (b) Figure 7: Osteoarthritis with the deformed articular surface of the condyle with a large anterior marginal osteophyte and deformed disc with central thinning on (a) MR and (b) ultrasound. A focal annotated view was provided to aid visualization with the articular disc outlined with a dotted contour and the osteophyte indicated by an arrow; anterior � “ANT”; condyle � “c.” visualize cortical osseous defects including osteophytes and (1) Ultrasound should currently be limited to use as an erosions. Retrodiscal visualization with US may partially be initial screening tool, and the sonologist needs to limited by patient body habitus and permitted acoustic only detect if the exam is normal or abnormal. windows by the adjacent osseous structures. (2) If found to be normal, and surgery is not contem- Disadvantages of US include the previously mentioned plated, then no further investigation is deemed difficulties in visualizing medial and lateral disc displace- necessary. ments. While disc thickness and shape can be assessed with (3) If found to be abnormal, the patient should be re- US, perforations and adhesions will not be adequately visu- ferred for MRI. alized. Subcortical osseous abnormalities also cannot be vi- (4) Due to poor sensitivity in visualizing medial disc sualized. US always carries the inherent operator dependence, displacement, if suspected, MRI should be per- and there is necessarily a learning curve before an operator formed despite a normal screening US. will obtain the expertise required to match the results pre- sented in this paper. Our study is also limited to conventional US and MRI reconstruction algorithms. Others have evalu- Data Availability ated enhancement filters for possible improvement of diag- A summary of image interpretation is provided with ap- nostic efficiency on MRI [18], and similar evaluation on US is propriate data provided in the manuscript. Select images are a possible topic for future research. provided in the manuscript. Each individual case image is Our referring clinicians have stressed the importance of not available. TMJ imaging to help differentiate between early and late changes. Early changes tend to be limited to disc displacement only, while late changes tend to include osseous remodelling, Conflicts of Interest which may be underestimated or not assessed despite the advanced experience of the clinician. Fixed versus reducible ,e authors declare that they have no conflicts of interest. disc displacements were important to them for treatment planning. For fixed disc displacement, our clinicians focus on Acknowledgments mobilization of the joint, while reducible displacements are usually treated with bite splints. Surgery was not a common ,e authors thank Judy Rubin for the illustration in Figure 2. treatment option in their practices. We believe that US ultimately has a role beyond screening References for further MRI evaluation and can be used for definitive diagnosis in the majority of cases; however, definitive validation [1] J. M. H. Dibbets and L. T. van der Weele, “Prevalence of TMJ will likely require further evaluation using a larger sample size symptoms and X-ray findings,” European Journal of Ortho- dontics, vol. 11, no. 1, pp. 31–36, 1989. and hopefully a randomized prospective study in which pa- [2] P. L. Westesson and S. L. 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Cronan, “Pilot study to show the feasibility of high-resolution sagittal ultrasound imaging of the temporomandibular joint,” Journal of Oral and Maxil- lofacial Surgery, vol. 75, no. 6, pp. 1151–1162, 2017. [15] N. Su, A. J. van Wijk, C. M. Visscher, F. Lobbezoo, and G. J. M. G. van der Heijden, “Diagnostic value of ultraso- nography for the detection of disc displacements in the temporomandibular joint: a systematic review and meta- analysis,” Clinical Oral Investigations, vol. 22, no. 7, pp. 2599–2614, 2018. [16] S. M. Shaffer, J.-M. Brismee, ´ P. S. Sizer, and C. A. Courtney, “Temporomandibular disorders—part 1: anatomy and ex- amination/diagnosis,” Journal of Manual & Manipulative ?erapy, vol. 22, no. 1, pp. 2–12, 2014. [17] R. W. Katzberg, P.-L. Westesson, R. H. Tallents, and C. M. Drake, “Anatomic disorders of the temporomandibular joint disc in asymptomatic subjects,” Journal of Oral and Maxillofacial Surgery, vol. 54, no. 2, pp. 147–153, 1996. [18] G. A. Montesinos, S. L. P. 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Advanced Ultrasound Screening for Temporomandibular Joint (TMJ) Internal Derangement

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Abstract

Hindawi Radiology Research and Practice Volume 2020, Article ID 1809690, 10 pages https://doi.org/10.1155/2020/1809690 Research Article Advanced Ultrasound Screening for Temporomandibular Joint (TMJ) Internal Derangement 1 2 3 3 Saul N. Friedman , Miriam Grushka, Hussam K. Beituni, Madhu Rehman, 4 3 Hart B. Bressler , and Lawrence Friedman Division of Nuclear Medicine, Mallinckrodt Institute of Radiology, Washington University School of Medicine, Saint Louis, MO 63110, USA 974 Eglington Avenue West, Toronto, Ontario M6C 2C5, Canada Department of Medical Imaging, North York General, 4001 Leslie Street, Toronto, Ontario M2K 1E1, Canada Department of Family and Community Medicine, University of Toronto, Mount Sinai Hospital, 600 University Ave, Toronto, Ontario M5G 1X5, Canada Correspondence should be addressed to Saul N. Friedman; saul.friedman@gmail.com Received 25 December 2019; Accepted 17 February 2020; Published 4 May 2020 Academic Editor: Henrique M. Lederman Copyright © 2020 Saul N. Friedman et al. ,is is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Purpose. To present an advanced ultrasound (US) technique and propose its use as a screening diagnostic tool for temporo- mandibular joint (TMJ) internal derangement. Materials and Methods. ,e technique is based on maintaining the US probe parallel to the articular disc, rather than traditional axial and coronal views, with the position described relative to a clock face. Validation was achieved by direct comparison with magnetic resonance imaging (MRI). A total of 61 patients, with age ranging from 13 to 67 years, were prescreened for TMJ pain and internal derangement, underwent US imaging for screening, and MRI evaluation for final diagnosis. Results. 29 of the 61 patients had disc pathology on MRI. US screening produced no false positive results and only 6 false negative results, corresponding to a sensitivity of 79% and specificity of 100%. Half of the false negative cases involved disc pathology with a medial component to the disc displacement. Conclusion. US is both a sensitive and a specific screening tool for TMJ dysfunction when used by an appropriately trained operator, with the exception of medially displaced discs. If TMJ assessment is found to be abnormal, the patient should be referred for MRI, and any patient scheduled for surgery must have the diagnosis confirmed by MRI. If a component of medial disc displacement is suspected, MRI should be performed despite a normal screening US. examination, however, takes 20 to 45 minutes on average to 1. Introduction perform depending on the scanner and protocol, and pa- In the past, internal derangement of the temporomandibular tients have difficulty keeping still and having their mouths joint (TMJ) has been assessed with plain film radiographs as open for extended periods of time, especially if they are the initial investigation [1] followed by arthrography [2] and experiencing pain. In addition, the examination is costly and computed tomography (CT) [3]. More recently, magnetic access is still limited in many centres. Many patients also resonance imaging (MRI) [4–7] has provided a noninvasive experience claustrophobia and are unable to complete or accurate method of assessing the TMJ without associated even undergo the examination. radiation risks. Its advantages over previous methods in- Ultrasound is relatively inexpensive, is readily accessible, clude its ability to directly visualize the disc and accurately and can be performed in most outpatient facilities; studies determine the position of the disc with respect to the condyle take only an average of 10 to 15 minutes in total, and it is of the mandible and eminence of the temporal bone. ,e without any known risks. In addition, US provides the 2 Radiology Research and Practice opportunity to converse with patients and identify the exact 2.1. Ultrasound Technique Details. ,e patient can be in a locations of pain, while the probe can be used as a palpable sitting position or lying down on a stretcher. We prefer the tool for real-time identification of crepitus, clicking, motion, patients lying supine with the jaw tilted away from the side to and snapping sensations. ,e disadvantages of US remain be examined, as this position not only offers more stability the long learning curve and the fact that the test is operator for probe positioning but also allows for further patient dependent. ,ere is also the question of ultrasound being comfort. ,e joint is then palpated while we have the patient effectively used as a diagnostic tool [8–13], given the many open and close their mouth. Once the joint is located, the constraints that will be discussed. In particular, Katzberg probe is placed over the joint using a liberal amount of warm [12] questioned its validity stating that ultrasound images do gel. not appear to be anatomically correct, that tissues indicated Traditional ultrasound techniques have included posi- to be discs were not convincing, and that interpretation was tioning of the probe on the skin surface in the axial not blinded. He also believed that given the bone blockade (Figure 1(a)) and coronal (Figure 1(b)) planes [12, 13]. We barrier and inability of the ultrasound beam to bend around employ a method whereby the position of the probe can be curved narrow structures, ultrasound does not allow for compared to that of a clock face in a clockwise rotation. ,e adequate diagnosis. However, more recently, Katzberg and probe is angled appropriately parallel to the right disc in the colleagues have proposed the use of sagittal transoral US to sagittal plane initially at an angle 50–60 down from the evaluate the TMJ [14]. horizontal as measured from the anterior side of the probe or Additional and more recent works by numerous in- 5 o’clock in the closed-mouth position on the right vestigators provide strong support for the use of conven- (Figure 1(c)), followed by 0 angulation or 3 o’clock in the tional US techniques. For example, Li et al. [13] in 2012 semiopen position (Figure 1(d)), and finally an anterior calculated a sensitivity and specificity of 76% and 82% for angle of 50–60 up from the horizontal as measured from the disc displacement with reduction, respectively, and 79% and anterior side of the probe or 1 o’clock in the fully open- 91% without disc reduction, respectively. ,ey also stated mouth position on the right (Figure 1(e)). In a similar that ultrasound is acceptable as a rapid initial method to manner, these angles would correspond to 7 o’clock, 9 exclude some potential patients but recommended MRI if o’clock, and 11 o’clock positions, respectively, when in- treatment is necessary. In addition, they noted that the vestigating the left TMJ. Dynamic video clips of movement ability to diagnose lateral and posterior displacements by can be obtained by swivelling the probe or by keeping the ultrasound is not clear. More recently, Su et al. published a probe just off the horizontal, which varies from patient to meta-analysis in 2018 noting an overall sensitivity and patient. specificity of 75–81% and 73–80%, respectively, for disc ,e disc was considered normal in the static closed- displacement in the closed-mouth position and 65–74% and mouth position if the intermediate zone or centre of the 86–91%, respectively, for disc displacement in the open- hypoechoic disc was located between the anterosuperior mouth position [15]. aspect of the condyle and the posteroinferior aspect of the Katzberg [12] attempted to quantify the distribution of disc articular eminence. During movement, the disc was con- displacements in a prospective study of 76 volunteers and 102 sidered normal if the intermediate zone or centre of the disc patients studied with MRI. He noted 52% of abnormal joints maintained its central location to the condyle from the had anterior displacement, 27% of abnormal joints had closed-mouth to fully open-mouth positions. All other disc anteromedial displacement, 12% of abnormal joints had medial locations were considered to exhibit either anterior or displacement, 34% of abnormal joints had anterolateral dis- posterior displacement. placement, and 4% of abnormal joints had lateral displacement. He also stated that anteromedially and medially displaced discs, 2.2. Imaging Equipment. Ultrasound images were obtained totalling 39%, would not be visualized by ultrasound. using a 15–7 MHz L15-7io hockey stick transducer (Philips iU22 Ultrasound System, Netherlands). ,e total US image acquisition time was approximately 10 minutes per patient. 1.1. Goal. Using knowledge of the normal US appearance and MRI was performed using T1 coronal and sagittal images dynamic motion of the articular disc, we present a new tech- in both open- and closed-mouth positions as well as gradient nique for visualization and assessment of the TMJ using ul- kinetic dynamic sagittal images (GE Signa HDxt 1.5T, trasound, where the probe is positioned parallel to the disc Milwaukee, USA) with the following parameters: coronal throughout movement; this technique differs from traditional T1-weighted images with repetition time (TR) = 405 ms and vertical and horizontal probe positioning, where the focus has echo time (TE) = 10 ms, sagittal proton-density-weighted been on obtaining true axial and coronal plains of imaging. MRI images with TR = 2025 ms and TE = 30 ms, and sagittal T2 - of the TMJ is used as the gold standard for technique validation. weighted kinematic dynamic images with TR = 100 ms and TE = 10 ms. ,e total acquisition time was approximately 2. Materials and Methods 30 minutes per patient. Institutional review board approval from North York General Ethics Committee was obtained, and verbal consent 2.3. Validation with Normal Volunteers. Normal anatomy was obtained from all patients and subjects prior to inclusion was first reviewed through the evaluation of both TMJs in 10 in the study. normal volunteers between the ages of 20 and 30 years. Radiology Research and Practice 3 (a) (b) (c) (d) (e) Figure 1: Position of the probe on the skin surface for traditional (a) transverse and (b) coronal scans. ,e probe position during routine interrogation of the TMJ is (c) angled parallel to the disc in the sagittal plane at 50–60 below the horizontal as measured from the anterior side of the probe or 5 o’clock position in the closed-mouth position on the right, (d) angled parallel to the disc or 3 o’clock position in the half-open-mouth position on the right, and (e) angled 50–60 above the horizontal as measured from the anterior side of the probe in the fully open-mouth or 1 o’clock position on the right. In a similar manner, these angles represent 7 o’clock, 9 o’clock, and 11 o’clock positions when investigating the TMJ on the left. 2.4. Assessment of Patient Pathology. Patients were pre- delay in patient care. ,e same senior MSK radiologist with screened for TMJ pain and internal derangement based on over 20 years of specialized US MSK training performed all the history and clinical exam by our TMJ pathology spe- US interpretations. To avoid recall bias, the US reader cialist (author MG) or our pain specialist with particular remained blinded to all MRI results performed by other experience in TMJ pathology (author HBB). Recommen- readers. In addition, in the situation where the US reader dations on the physical exam technique have been described also interpreted the MRI first, a period of 3-4 weeks was in detail elsewhere [16]. A total of 61 symptomatic patients waited after the MRI interpretation before interpreting the were recruited, of which 43 were male and 18 female with a associated US. mean age of 40 years and age range of 13 to 67 years. MR and ,e US screen was considered positive if displacement US imaging was obtained using the same equipment and was observed, regardless of the direction (anterior, posterior, protocol as above. All US images were acquired by the senior medial, or lateral) and regardless of whether it reduced or radiologist (author LF), who had over 20 years of specialized remained fixed. In cases where displacement was observed in US MSK experience. Contrast was not used for either MR or multiple directions (e.g., anteromedial), the displacement US imaging. MRI interpretations were performed by 4 ra- was labelled by the predominant direction of displacement. diologists, each with a minimum of 5 years of experience Pathology was then further subdivided into fixed displace- working in a practice, and typically completed first to avoid ment and recapture subgroups. Osteoarthritic changes and 4 Radiology Research and Practice Figure 2: Normal anatomy illustrating the condyle of the mandible, superior and inferior belly of the lateral pterygoid muscle, articular disc, articular eminence of the temporal bone, and articular fossa (glenoid fossa) of the temporal bone. evidence of inflammation as determined through increased closely applied cortical surface of the condyle and the blood flow were also evaluated but could only be performed eminence. Close attention to this relationship is critical in on US as MRI postcontrast imaging was not performed. separating a normal from an abnormal disc on both MRI and ultrasound interrogation. For a right-sided TMJ in the closed-mouth position in the sagittal plane, the anterior 3. Results angle of the normal disc is 50–60 down from the hori- 3.1. Normal TMJ. A diagram of basic anatomy is presented zontal. When midway between open- and closed-mouth in Figure 2 as a visual aid. ,e articular disc in the normal positions, the anterior angle is 0 to the horizontal, and in TMJ is a fibrous structure composed of a superficial band, a the fully-open-mouth position, it is 50–60 up from the slightly more thickened deep band, and a very thin inter- horizontal. ,e mirror image configuration is present in the mediate zone that is attached posteriorly to the temporal left-sided TMJ. bone through the bilaminar zone and anteriorly to the lateral pterygoid muscle superior belly. A lower synovial-lined joint space separates it from the head of the condyle, and a 3.2. Abnormal TMJ. Pathology for the 61 patients included noncommunicating upper joint separates it from the bony in the study as determined by MRI is summarized in glenoid fossa and the articular eminence of the temporal Table 1. ,e 29 patients positive for TMJ pathology cor- bone. respond to a prevalence of 47.5%. Fixed posterior dis- On MRI, the disc has a bowtie or saddle appearance. On placement was not observed. Of the 14 patients with fixed sonography, a normal disc usually appears as an inverted anterior displacement, 3 were noted to have a medial more hypoechoic c-shaped structure that straddles the component to the displacement. Lateral disc displacement hyperechoic cortex of the condyle, as seen in Figure 3. was not observed. However, the disc can also appear isoechoic to hyperechoic Ultrasound screening identified 23 of the 29 patients especially as it becomes less hydrated and more calcified with with pathology, corresponding to 6 false negatives. No false disease. positive results were obtained. ,is corresponds to a sen- During normal movement and disc translation, the disc sitivity of 79% and specificity of 100%; results are sum- maintains a constant relationship between the condyle marized in Table 2. ,e 6 false negative cases all head of the mandible and the eminence of the temporal corresponded to fixed anterior displacement and included bone. From the closed-mouth to the fully-open-mouth all 3 cases that were noted to contain a medial component of position, the thin intermediate zone should be between the displacement. Based on the calculated prevalence of 47.5%, Radiology Research and Practice 5 Figure 3: Normal ultrasound appearance of the articular disc in the sagittal plane, seen as an inverted hypoechoic c-shaped structure. Note that the disc maintains a constant central appearance with respect to the centre of the condyle, “c,” outlined by a central vertical line during the closed-mouth, half-open-mouth, and fully-open-mouth views. ,e anterior (“ant”) band and posterior band of the articular disc appear symmetrical in size with respect to the centre of the condyle. A focal annotated view was provided to aid visualization with the articular disc outlined with a dotted contour. the calculated positive predictive value is 100% and the fixed anterior dislocation, is demonstrated in Figure 5. While negative predictive value is 84%. the morphology of the disc usually remains normal with US and MRI of anterior disc displacement with recapture an anteriorly displaced disc that recaptures, it more often of the disc in the open-mouth position are demonstrated in appears morphologically abnormal with fixed anterior Figure 4. Note the normal MRI bowtie appearance in Figure dislocation, as noted in Figure 5. Posterior displacement 4(b). Corresponding pathology without recapture, labelled as is demonstrated in Figure 6. Bony deformity and bony 6 Radiology Research and Practice Table 1: A total of 29 of the 61 patients experiencing temporomandibular symptoms had pathology visible on magnetic resonance imaging (MRI), corresponding to a disease prevalence of 47.5%. Pathology is subdivided into anterior, posterior, and medial displacements and summarized here, with the number demonstrating the presence of recapture, osteoarthritic changes, and presence of inflammation (as determined from ultrasound imaging) noted. Pathological disc displacement Fixed Recapture present Total Anterior 14 14 28 Posterior 0 1 1 Medial 0 0 0 Lateral 0 0 0 Total 14 15 29 3 cases were further noted to have a medially displaced component. Table 2: Summary of results of the 61 patients prescreened for temporomandibular symptoms using ultrasound (US) and compared to the gold standard of magnetic resonance imaging (MRI). US results are split into true positive and true negative (concordant with MRI), and false positive and false negative (discordant with MRI), corresponding to a sensitivity of 79% and specificity of 100%. MRI screened positive MRI screened negative US screened positive 23 0 US screened negative 6 32 (a) (b) (c) (d) Figure 4: Images demonstrating anterior displacement of the disc in the sagittal plane in the (a) closed-mouth position with MR, (b) disc recapture in the open-mouth position with MR, (c) closed-mouth position with US, and (d) recapture in the open-mouth position with US. ,e disc retains normal morphology. A focal annotated view was provided to aid visualization with the articular disc outlined with a dotted contour; condyle � “c”; eminence � “e”; anterior � “ant.” Radiology Research and Practice 7 (a) (b) (c) (d) Figure 5: Images demonstrating a deformed disc with fixed anterior dislocation in the sagittal plane in the (a) closed-mouth position with MRI, (b) open-mouth position with MRI, (c) closed-mouth position with US, and (d) open-mouth position with US. A focal annotated view was provided to aid visualization with the articular disc outlined with a dotted contour; condyle � “c”; anterior � “ant”; left � “LT.” (a) (b) Figure 6: Continued. 8 Radiology Research and Practice (c) (d) Figure 6: Images demonstrating posterior displacement of the disc in the (a) closed-mouth position with MRI, (b) recapture in the open- mouth position with MRI, (c) closed-mouth position with US, and (d) recapture in the open-mouth position with US. A focal annotated view was provided to aid visualization with the articular disc outlined with a dotted contour; anterior � “ant”; condyle � “c”; left � “LT.” likely imaging prevalence. While the power of our study is osteophyte formation in osteoarthritis involving the condyle can be visualized on ultrasound, as demonstrated limited, we believe our results to be sufficient for the initial validation of US as a screening tool to help decide who in Figure 7. should proceed with additional MRI. We continue to screen patients with our US technique and have evaluated 4. Discussion more than 350 additional patients; however, lack of cor- We introduce an advanced technique for evaluating the responding MRI evaluation prevented their inclusion in temporomandibular joint through ultrasound imaging this study. by positioning the probe parallel to the articular disc Ethical management, requiring a definitive diagnosis for throughout dynamic motion. US was presented as a treatment to not be delayed, prevented US image acquisition screening tool for TMJ dysfunction due to its ubiquitous and interpretation prior to MRI evaluation. Potential bias was minimized by limiting the number of MRIs interpreted nature and relatively inexpensive cost. MRI was chosen as the gold standard for comparison due to its high level by the expert radiologist who interpreted the US studies, and keeping him ignorant of MRI results until assessment of the of specificity and sensitivity, as well as its role in current standard of practice. US images was completed. In cases where the MRI was read We have limited our description of articular disc pa- first by the same radiologist who read the subsequent US, the thology to anterior, posterior, medial, and lateral dislo- US interpretation was held for 3-4 weeks to minimize recall cation, based on the most prominent feature only. While bias. this creates labelling bias, this is unlikely to affect the Of the 6 false negative cases obtained using our tech- patient outcome as the primary role is screening and nique, all cases noted to involve medial disc displacement subsequent MRI studies were performed for further were included. ,is is likely due to the limited penetrance of characterization. Lateral displacement was not visualized US because of bone and other anatomy, restricting it to the superficial one-third of the disc. Others have also noted that in our study; however, this is not unexpected. Based on the 4% prevalence of lateral displacement by Katzberg et al. laterally or medially displaced discs are known to be in- adequately visualized and evaluated with present ultrasound [17], only a single case is expected within a group of 29, and random chance alone is enough to explain its absence. techniques [13]. However, medial and lateral displacements were generally Advantages of US over MRI identified during our study difficult to visualize on US and are likely underestimated include the ability to observe real-time motion, clicking based on US alone. Validation of lateral displacement on and crepitus, the ability to localize imaging to patient- US will require a much larger sample size given the relative directed regions of pain, and the ability to evaluate patients rarity. who are claustrophobic or have stents and implants that are Prescreening patients for TMJ symptoms inherently not MRI compatible. Doppler imaging enabled us to di- creates a selection bias, with our measured prevalence of agnose inflammation by the presence of abnormal blood flow that, while theoretically possible if contrast is used, is 47.5% grossly overestimating prevalence in the general population, but reflecting realistic clinical practice and the unlikely on MRI with standard practices. US is also able to Radiology Research and Practice 9 (a) (b) Figure 7: Osteoarthritis with the deformed articular surface of the condyle with a large anterior marginal osteophyte and deformed disc with central thinning on (a) MR and (b) ultrasound. A focal annotated view was provided to aid visualization with the articular disc outlined with a dotted contour and the osteophyte indicated by an arrow; anterior � “ANT”; condyle � “c.” visualize cortical osseous defects including osteophytes and (1) Ultrasound should currently be limited to use as an erosions. Retrodiscal visualization with US may partially be initial screening tool, and the sonologist needs to limited by patient body habitus and permitted acoustic only detect if the exam is normal or abnormal. windows by the adjacent osseous structures. (2) If found to be normal, and surgery is not contem- Disadvantages of US include the previously mentioned plated, then no further investigation is deemed difficulties in visualizing medial and lateral disc displace- necessary. ments. While disc thickness and shape can be assessed with (3) If found to be abnormal, the patient should be re- US, perforations and adhesions will not be adequately visu- ferred for MRI. alized. Subcortical osseous abnormalities also cannot be vi- (4) Due to poor sensitivity in visualizing medial disc sualized. US always carries the inherent operator dependence, displacement, if suspected, MRI should be per- and there is necessarily a learning curve before an operator formed despite a normal screening US. will obtain the expertise required to match the results pre- sented in this paper. Our study is also limited to conventional US and MRI reconstruction algorithms. Others have evalu- Data Availability ated enhancement filters for possible improvement of diag- A summary of image interpretation is provided with ap- nostic efficiency on MRI [18], and similar evaluation on US is propriate data provided in the manuscript. Select images are a possible topic for future research. provided in the manuscript. Each individual case image is Our referring clinicians have stressed the importance of not available. TMJ imaging to help differentiate between early and late changes. Early changes tend to be limited to disc displacement only, while late changes tend to include osseous remodelling, Conflicts of Interest which may be underestimated or not assessed despite the advanced experience of the clinician. Fixed versus reducible ,e authors declare that they have no conflicts of interest. disc displacements were important to them for treatment planning. 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Radiology Research and PracticeHindawi Publishing Corporation

Published: May 4, 2020

References