Clin Oral Invest (2014) 18:1865–1871 DOI 10.1007/s00784-013-1154-5
ORIGINAL ARTICLE
Biochemical analysis of the articular disc of the temporomandibular joint with magnetic resonance T2 mapping: a feasibility study Martina Schmid-Schwap & Margit Bristela & Elisabeth Pittschieler & Astrid Skolka & Pavol Szomolanyi & Michael Weber & Eva Piehslinger & Siegfried Trattnig
Received: 16 January 2013 / Accepted: 20 November 2013 / Published online: 5 December 2013 # Springer-Verlag Berlin Heidelberg 2013
Abstract Objectives Symptoms of temporomandibular joint (TMJ) dysfunction can seriously compromise patients' quality of life. The aim of our study was to use magnetic resonance imaging (MRI) T2 mapping of the articular disc to determine whether T2 mapping of the TMJ disc is feasible in routine clinical imaging and to assess the normal T2 relaxation time distribution within the TMJ. Methods Included were ten asymptomatic volunteers without pain, any mouth-opening limitations, or any
clicking phenomena. MR imaging was performed on a 3-T MR scanner using a flexible, dedicated, eightchannel multielement coil. T2 mapping was performed in the oblique sagittal plane. The regions of interest (ROIs) for the T2 relaxation time maps of the disc were selected manually. Results The mean values for ROIs ranged between 22.4 and 28.8 ms, and the mean for all ROIs was 26.0± 5.0 ms. Intraclass correlation (ICC) for interobserver variability was 0.698, and ICC for intraobserver variability was 0.861. There
M. Schmid-Schwap (*) : M. Bristela : A. Skolka : E. Piehslinger Department of Prosthodontics, Bernhard Gottlieb University of Dentistry, Medical University of Vienna, Sensengasse 2a, 1090 Vienna, Austria e-mail: [email protected]
P. Szomolanyi Department of Imaging Methods, Institute of Measurement Science, Slovak Academy of Sciences, Dubravska cesta 9, 84219 Bratislava, Slovakia
M. Bristela e-mail: [email protected] A. Skolka e-mail: [email protected] E. Piehslinger e-mail: [email protected] E. Pittschieler Department of Orthodontics, Bernhard Gottlieb University of Dentistry, Medical University of Vienna, Sensengasse 2a, 1090 Vienna, Austria e-mail: [email protected]
M. Weber Department of Biomedical Imaging and Image-Guided Therapy, Medical University of Vienna/Vienna General Hospital, Waehringer Guertel 18-20, 1090 Vienna, Austria e-mail: [email protected]
P. Szomolanyi : S. Trattnig High Field MR Centre, Department of Biomedical Imaging and Image-Guided Therapy, Medical University of Vienna/Vienna General Hospital, Waehringer Guertel 18-20, 1090 Vienna, Austria P. Szomolanyi e-mail: [email protected] S. Trattnig e-mail: [email protected]
S. Trattnig Austrian Cluster for Tissue Regeneration, Ludwig Boltzmann Institute for Experimental and Clinical Traumatology, Donaueschingenstrase 13, 1200 Vienna, Austria
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was no statistically significant difference between raters (p = 0.091) or sides (p =0.810). Conclusion The T2 mapping technique enables ultrastructural analysis of the composition of TMJ disc. This biochemical technique is feasible in vivo, as shown in our study, when a high-field (3 T) MR and a dedicated TMJ coil are used. Clinical relevance T2 mapping as a biochemical technique, together with morphological MRI, may help to gain more insights into the physiology and into the pathophysiology of the articular disc in the TMJ noninvasively and in vivo.
knowledge, there is only one case report on TMJ and biochemical imaging techniques [14], and there are no reports that investigate T2 mapping of the TMJ structures in the peerreviewed literature. The aim of our study was to evaluate T2 mapping of the articular disc in ten healthy volunteers to address the following issues: first, is T2 mapping of the TMJ disc feasible in routine clinical imaging? Second, what is the normal T2 relaxation time distribution within the TMJ?
Keywords MRI . 3 T . T2 mapping . Temporomandibular joint . Articular disc
Materials and methods Volunteer selection
Introduction Dysfunction and displacement of the articular disc are very common disorders of the temporomandibular joint (TMJ). Patients describe pain and clicking phenomena as primary symptoms. The pain associated with temporomandibular disorders has a substantial impact on patients' quality of life [1]. The cartilage and the articular disc are crucial to the functioning of the joint (motion, absorption of mastication, and parafunctional forces). For the visualization of morphological joint changes, magnetic resonance imaging (MRI), in contrast to plain radiographs, is a valuable tool [2, 3], particularly on MR scanners operating at high field strengths [4, 5]. MRI enables the visualization and delineation of various tissues within the TMJ, such as cartilage and the articular disc, as opposed to conventional radiography, which is limited to the assessment of the narrowing of the joint space or coarse osseous changes. In addition to the displacement of the disc, MRI can characterize the shape and signal intensity of the articular disc, but in morphological images, the opportunities are limited to evaluating the ultrastructure of the articular disc of TMJ. Only the signal intensity can reflect structural changes of the disc. Therefore, biochemical imaging techniques, in combination with a high-field strength MR scanner of a minimum of 3 T, may add a diagnostic value for the detection of lesions at an early stage. A widely used biochemical MR imaging technique is T2 mapping. This technique uses T2 relaxation times as an indirect indicator of structural changes in the cartilage collagen fiber organization and network. The interaction between water molecules and collagen fibers is used to visualize the collagen organization, extracellular matrix structure, and water content [6]. A change in T2 values can indicate early structural changes. The use of contrast agents is not necessary; thus, T2 mapping has been used in many studies of various joints, mostly for the evaluation of articular cartilage in patients with osteoarthritis and in patients after different cartilage repair surgery techniques, and in other tissues such as the intervertebral disc [7–13]. To the best of our
All experiments were performed in accordance with the ethical standards of the World Medical Association (Declaration of Helsinki). The approval of the ethics committee was obtained before the examination of the volunteers. All volunteers gave written, informed consent to use their anonymized data. Between October 2010 and July 2011, 14 volunteers were recruited. Twenty joints from ten volunteers were included in the study. Six volunteers were female, and four were male. The mean age (±standard deviation) was 26.1±6.6 years (range, 20 to 43). All volunteers underwent a clinical examination, including measurement of the mouth opening and palpation of the temporomandibular joint and muscles. Included were volunteers without pain, who had no mouthopening limitations, no clicking phenomena, and no anterior disc displacement in the temporomandibular joints. Exclusion criteria were age younger than 18 and older than 50 years; fixed orthodontic device; metallic foreign bodies in the head region; presence of biostimulators (pacemaker, insulin pump, etc.) and other contraindications to MR, such as claustrophobia, tremor, or other forms of motor unrest; and pregnancy. Two volunteers failed to appear for the MRI examination, one volunteer was excluded due to reciprocal clicking, and one volunteer had to be excluded because of anterior disc displacement without reduction. Magnetic resonance imaging MR imaging was performed on a 3-T MR scanner (Magnetom TIM Trio, Siemens Healthcare, Erlangen, Germany) using a flexible, dedicated, eight-channel multielement coil (Noras, Würzburg, Germany). For all volunteers, both joints were imaged simultaneously in the supine position with the mouth in the closed position (Fig. 1). In addition, images with the mouth in an opened position were obtained using standardized wedge blocks with a thickness of 25 mm. For the morphological evaluation of the disc position and rating of the perceptibility, we used oblique sagittal and oblique coronal slice orientations. MR sequences and imaging parameters are listed
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Fig. 1 Example of T2-weighted image (oblique sagittal, closed mouth) of the right TMJ of one volunteer
in Table 1. The technique used for T2 mapping of cartilage was a multiple spin-echo Carr–Purcell–Meiboom–Gill (CPMG) sequence [15, 16]. This sequence typically yields a series of T2-weighted images with variable echo times, which can be further post-processed into T2 maps.
sagittal and coronal slices in the opened and closed positions. All examiners assessed the images of the mouth in the closed position independently of each other, according to the perceptibility of position/delineation to surrounding tissue and morphology of the disc, using a five-point scale (1=excellent delineation with sharply defined border lines, 5=insufficient delineation, structures not circumscribable). The changes in the signal (evenly dark/central brightening/focal brightening/ disc residues) and morphology (biconcave/flattened/biconvex/deformed) of the disc were also evaluated [5]. The regions of interest (ROIs) for the T2 relaxation time maps were selected manually by each examiner. For the ROI of the TMJ disc, the contour of the disc and the anterior, central, and posterior part of the disc were drawn on the image that revealed the best morphological contrast and transferred via “copy and paste” into the T2 map (Fig. 2). To assess intraobserver reproducibility, these measurements were repeated after at least 4 weeks by the same investigator (M.S.), and to assess interobserver agreement, by the two other observers (M.B. and A.S.). The evaluation was performed at the Department of Radiology, under the supervision of a radiologist with 20 years of experience in clinical and experimental MR research and diagnostics.
Image analysis Statistical analysis Three experienced examiners who specialized in temporomandibular disease (TMD) therapy [M.S. (20 years experience), M.B. (more than 10 years of experience), and A.S. (more than 5 years of experience) in TMJ dysfunction syndrome treatment] were blinded to volunteer identity. One examiner (M.S.) assessed the normal location and position of the condyle and the disc on the morphological, oblique Table 1 MR measurement parameters for Carr–Purcell– Meiboom–Gill (CPMG), proton density (PD), and morphological dual-echo steady state (DESS) protocol
All statistical evaluations were performed using IBM SPSS Statistics version 19.0. Metric data, such as T2 values, are presented using mean ± SD. To assess the reproducibility of T2 evaluation, interobserver variability was calculated from three different evaluations in each region (ROIs 1–4) by three experienced independent raters. Results were expressed as CPMG Parasagittal (closed position)
DESS Coronal
PD Parasagittal (opened position)
FOV (mm × mm) Number of slices (left + right) Slice thickness (mm) Slice separation (mm) Number of averages TR (ms) TE (ms) Echo train
155×155 6+6 2 2.2 1 1,440 100.8 10
162×192 – 0.60 – 2 15.16 4.37 1
90×90 11+11 2 2.2 1 1,810 30 1
Total acquisition time (min/s) Acquisition matrix (pix) Percent phase field of view (%) Percent sampling (%) Pixel bandwidth (Hz/pix) MR acquisition type Reconstructed matrix (pix) Pixel spacing (mm)
14:47 384×384 100 100 200 2D 384×384 0.40×0.40
21:14 378×448 84.375 100 169 3D 756×896 0.21×0.21
4:56 384×384 100 100 161 2D 768×768 0.12×0.12
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Clin Oral Invest (2014) 18:1865–1871 Table 2 Summarized mean values ± std. deviation of ROI evaluations. ROI 1 includes the entire disc, ROI 2 includes the anterior part of the disc, ROI 3 includes the central part of the disc, and ROI 4 includes the posterior part of the disc. Each ROI was evaluated by three raters (left side, N =30; right side, N =30; both sides, N =60) Evaluator
Side
ROI
Mean
Std. deviation
No.
Total
Left
1
26.9
3.2
30
2 3 4 1 2 3 4 1 2 3 4
26.5 25.9 24.3 27.0 28.8 26.1 22.4 26.9 27.6 26.0 23.4
5.8 2.7 2.6 4.2 8.4 5.3 2.4 3.7 7.2 4.2 2.7
30 30 30 30 30 30 30 60 60 60 60
Right Fig. 2 Example of T2 map (oblique sagittal, closed mouth) of the TMJ of the selected volunteer shown in Fig. 1, with the ROIs delineated
intraclass correlation coefficients (ICCs). ICCs are based on all measurements per rater (one rater/ROIs 1–4, left/right side: N =80). In order to assess mean differences in T2 values between individual ROIs, a mixed model ANOVA was used, with an unstructured covariance matrix, taking into account multiple measures per volunteer. Bonferroni-corrected, pairwise post hoc comparisons were based on estimated marginal means. A value of p ≤0.05 was considered to indicate significant results.
Results All investigated joints demonstrated a normal condyle position and no anterior disc dislocation. Most of the discs showed normal signal intensity. Rater 1 diagnosed focal brightening of the disc in one volunteer (both sides), and rater 2 detected central brightening in one left joint and one right joint and focal brightening of the disc in one right joint. Rater 3 diagnosed one central brightening and one focal brightening in the right disc.
All joints
significant difference between raters (p =0.091) or sides (p = 0.810). When T2 values aggregated over both sides and the three raters were compared, post hoc tests revealed significant differences only between ROIs 1 and 4 (p =0.002).
Discussion Identifying possible predictors and risk factors for TMJ problems using MRI images remains a challenge. The risk of degenerative changes and joint effusion increases with displacement of the disc [17]. Joint effusion may be a predictor for the existence of synovitis [18–20]. Attempts have been made to correlate T2 signal values from T2-weighted images with symptoms of temporomandibular dysfunction. Sano and
Results of morphological assessment Mean values of a five-point scale (1=excellent to 5=very poor) for the perceptibility of position/delineation to surrounding tissue was (mean ± std. dev) 1.5±0.8 for the left side and 1.7±0.8 for the right side, and, for the morphology of the disc, 1.2±0.4 for the left side and 1.3±0.6 for the right side. Results of biochemical analysis (T2 relaxation time mapping) The mean values for the ROIs were between 22.4 and 28.8 ms, and the mean for all ROIs was 26.0±5.0 ms (Table 2). The ICC for interobserver variability was 0.698, and the ICC for intraobserver variability was 0.861. Figure 3 shows the results for all raters and ROIs. There was no statistically
Fig. 3 Mean T2 values for the different ROIs and the different raters. A clear tendency toward a decrease in T2 from the anterior to the posterior part of the disc is demonstrated
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Westesson found a correlation between TMJ pain and an increased T2-weighted signal in the retrodiscal tissue; however, no correlation between the T2 signal intensity and disc position could be found [21]. T2 mapping is regarded as a powerful technique that provides information about the status of the cartilage collagen network without the need for contrast agents [22]. This technique has been validated for the detection of collagen and may also be sensitive to proteoglycan, which was demonstrated in several studies investigating large joints, such as the knee [11, 22, 23]. The aim of this study was to evaluate whether T2 mapping of the articular disc of the temporomandibular joint is feasible and to assess the normal T2 relaxation time distribution within the TMJ to enable later patient studies using this biochemical technique. The presented work was intended as a “feasibility study.” Therefore, only ten asymptomatic volunteers (20 joints) were included in the study, and no power analyses were performed. The local ethics committee recommends ten cases, at most, for pilot (feasibility) studies. To the best of our knowledge, there are no reports in the literature about T2 mapping of the TMJ at 1.5 T. The signalto-noise ratio (SNR) of T2 mapping at 1.5 T is critical. Due to low SNR, the precision of the T2 values in the TMJ disc would be compromised, and this type of diagnostic technique would not be feasible. Several studies of the knee joints using T2 mapping at 1.5 T have been published [24–26]. The authors could find only one brief report dealing with T2 mapping of the TMJ [14]. Our study shows that T2 relaxation time measurements of the articular disc of the TMJ are feasible, with good inter- and intraobserver agreement. The highest T2 relaxation times were found in the anterior part of the articular disc, with lower T2 values in the central part of the disc, and the lowest values in the posterior part of the disc. As can be seen in histological specimens, in the anterior part of the disc, cross-sectioned collagen fiber bundles appeared thinner, and in the middle part, collagen fibers were more longitudinally sectioned and showed a more dense and organized orientation (Fig. 4). In contrast, the posterior part of the disc shows thicker collagen fiber bundles, mainly crosssectioned, strongly woven, and highly organized. Based on the histology, we can prove that the orientation of collagen fibers is not at the magic angle (54° 44′ relative to B0). Therefore, the magic angle effect, i.e., a local increase in the T2 relaxation time, is not observed in the TMJ disc. The MRI investigations were performed with the mouth in a closed position. It is possible that the decrease in values in the central, and particularly, in the posterior part, could have been caused by the greater pressure of the condyle in these regions. The interobserver agreement showed good reproducibility, with 0.7, and an intraobserver agreement greater than 0.8. The interclass agreement (0.8) for the whole disc was sufficient to reproducibly evaluate the T2 values of the disc. Figure 3 shows
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Fig. 4 Micromorphology of collagen fibers in the TMJ disc, using an undecalcified ground and polished section, after surface staining with Giemsa solution
a good inter-rater correlation for all ROIs, except for ROI 2 with rater 2. However, the absolute difference in T2 values was small and not statistically significant. The values for the central and posterior part of the disc showed a good intraclass correlation, with values greater than 0.8 and 0.7, respectively. It was surprising that ROI 2 did not differ from ROI 4, although the difference was larger than between ROIs 1 and 4. A possible reason may be that the variance in ROI 2 was larger than in any other ROI, indicating the most heterogeneous measurements within that ROI. A possible explanation for this is the morphology of the disc. The anterior part of the articular disc of the TMJ is usually larger than the central part and, in some cases, larger than the posterior part and thus shows a greater variety of T2 relaxation time values within the ROIs. Morphologically, the evaluated joints showed a normal condyle and disc position. The perceptibility of position/ delineation relative to surrounding tissue and of the morphology of the disc was rated as very good by all three raters. The limitation of the study is that only asymptomatic volunteers were enrolled. However, to assess the feasibility of T2 mapping in vivo and to become familiar with normal T2 relaxation time values in different regions of the healthy articular discs, a basic study with volunteers is necessary. Due to the limited number of volunteers in this study, more subjects should be studied to assess what is standard for the normal relaxation time distribution within the TMJ disc. Another limitation of the proposed technique is that it requires a high-field MR system operating at 3 T and a dedicated coil, which was available in the present study. The authors did not aim to bring this protocol into the clinic at the current stage. Therefore, a longer scan time was tolerated. In future studies, we will try to reduce measurement time in order to provide a clinically acceptable method. After further development, this method may be able to demonstrate lesions at a very early stage.
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The proposed T2 mapping technique with T2 relaxation time measurements enables an ultrastructural analysis of the composition of the articular disc of the TMJ. This biochemical technique is feasible in vivo, as shown in our study, when a high-field (3 T) MR and a dedicated TMJ coil is used, which provides sufficient signal-to-noise ratio to perform T2 mapping with reasonable resolution in a small structure like the TMJ disc. T2 mapping has the potential to provide additional information to standard morphological MR imaging, which may allow the diagnosis of early stages of disc degeneration before morphological changes occur. In addition, T2 mapping may be a sensitive tool for the monitoring of different therapies, both surgical and conservative, for various disorders of the TMJ. T2 mapping as a biochemical technique, together with morphological MRI, may help to gain more insights into the physiology and the pathophysiology of the articular disc in the TMJ, noninvasively, and in vivo. As a clinical diagnosis of TMJ is limited, MR, which can provide morphological and biochemical imaging, allows a more accurate analysis of TMJ disorders [2, 27–29].
Conclusion The T2 mapping technique enables ultrastructural analysis of the composition of the TMJ disc. This biochemical technique is feasible in vivo, as shown in our study, when a high-field (3 T) MR and a dedicated TMJ coil are used Acknowledgments This study was funded by the Austrian Science Fund FWF grant P23481-B19, Vienna Spots of Excellence of the Vienna Science and Technology Fund (WWTF), Vienna Advanced Imaging Center (VIACLIC FA102A0017), and grant VEGA 2/0013/14 of the Slovak Grant Agency. We would like to thank the volunteers, and we highly appreciate the technical support of Claudia Kronnerwetter. We would like to give a special thanks to Prof. Hanns Plenk from the Institute for Histology and Embryology/Medical University of Vienna and Prof. Monika Egerbacher from the Institute for Anatomy, Histology and Embryology of the University of Veterinary Medicine for their valuable support with the histological evaluation. Conflict of interest The authors declare that they have no conflict of interest.
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ORIGINAL ARTICLE
Biochemical analysis of the articular disc of the temporomandibular joint with magnetic resonance T2 mapping: a feasibility study Martina Schmid-Schwap & Margit Bristela & Elisabeth Pittschieler & Astrid Skolka & Pavol Szomolanyi & Michael Weber & Eva Piehslinger & Siegfried Trattnig
Received: 16 January 2013 / Accepted: 20 November 2013 / Published online: 5 December 2013 # Springer-Verlag Berlin Heidelberg 2013
Abstract Objectives Symptoms of temporomandibular joint (TMJ) dysfunction can seriously compromise patients' quality of life. The aim of our study was to use magnetic resonance imaging (MRI) T2 mapping of the articular disc to determine whether T2 mapping of the TMJ disc is feasible in routine clinical imaging and to assess the normal T2 relaxation time distribution within the TMJ. Methods Included were ten asymptomatic volunteers without pain, any mouth-opening limitations, or any
clicking phenomena. MR imaging was performed on a 3-T MR scanner using a flexible, dedicated, eightchannel multielement coil. T2 mapping was performed in the oblique sagittal plane. The regions of interest (ROIs) for the T2 relaxation time maps of the disc were selected manually. Results The mean values for ROIs ranged between 22.4 and 28.8 ms, and the mean for all ROIs was 26.0± 5.0 ms. Intraclass correlation (ICC) for interobserver variability was 0.698, and ICC for intraobserver variability was 0.861. There
M. Schmid-Schwap (*) : M. Bristela : A. Skolka : E. Piehslinger Department of Prosthodontics, Bernhard Gottlieb University of Dentistry, Medical University of Vienna, Sensengasse 2a, 1090 Vienna, Austria e-mail: [email protected]
P. Szomolanyi Department of Imaging Methods, Institute of Measurement Science, Slovak Academy of Sciences, Dubravska cesta 9, 84219 Bratislava, Slovakia
M. Bristela e-mail: [email protected] A. Skolka e-mail: [email protected] E. Piehslinger e-mail: [email protected] E. Pittschieler Department of Orthodontics, Bernhard Gottlieb University of Dentistry, Medical University of Vienna, Sensengasse 2a, 1090 Vienna, Austria e-mail: [email protected]
M. Weber Department of Biomedical Imaging and Image-Guided Therapy, Medical University of Vienna/Vienna General Hospital, Waehringer Guertel 18-20, 1090 Vienna, Austria e-mail: [email protected]
P. Szomolanyi : S. Trattnig High Field MR Centre, Department of Biomedical Imaging and Image-Guided Therapy, Medical University of Vienna/Vienna General Hospital, Waehringer Guertel 18-20, 1090 Vienna, Austria P. Szomolanyi e-mail: [email protected] S. Trattnig e-mail: [email protected]
S. Trattnig Austrian Cluster for Tissue Regeneration, Ludwig Boltzmann Institute for Experimental and Clinical Traumatology, Donaueschingenstrase 13, 1200 Vienna, Austria
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was no statistically significant difference between raters (p = 0.091) or sides (p =0.810). Conclusion The T2 mapping technique enables ultrastructural analysis of the composition of TMJ disc. This biochemical technique is feasible in vivo, as shown in our study, when a high-field (3 T) MR and a dedicated TMJ coil are used. Clinical relevance T2 mapping as a biochemical technique, together with morphological MRI, may help to gain more insights into the physiology and into the pathophysiology of the articular disc in the TMJ noninvasively and in vivo.
knowledge, there is only one case report on TMJ and biochemical imaging techniques [14], and there are no reports that investigate T2 mapping of the TMJ structures in the peerreviewed literature. The aim of our study was to evaluate T2 mapping of the articular disc in ten healthy volunteers to address the following issues: first, is T2 mapping of the TMJ disc feasible in routine clinical imaging? Second, what is the normal T2 relaxation time distribution within the TMJ?
Keywords MRI . 3 T . T2 mapping . Temporomandibular joint . Articular disc
Materials and methods Volunteer selection
Introduction Dysfunction and displacement of the articular disc are very common disorders of the temporomandibular joint (TMJ). Patients describe pain and clicking phenomena as primary symptoms. The pain associated with temporomandibular disorders has a substantial impact on patients' quality of life [1]. The cartilage and the articular disc are crucial to the functioning of the joint (motion, absorption of mastication, and parafunctional forces). For the visualization of morphological joint changes, magnetic resonance imaging (MRI), in contrast to plain radiographs, is a valuable tool [2, 3], particularly on MR scanners operating at high field strengths [4, 5]. MRI enables the visualization and delineation of various tissues within the TMJ, such as cartilage and the articular disc, as opposed to conventional radiography, which is limited to the assessment of the narrowing of the joint space or coarse osseous changes. In addition to the displacement of the disc, MRI can characterize the shape and signal intensity of the articular disc, but in morphological images, the opportunities are limited to evaluating the ultrastructure of the articular disc of TMJ. Only the signal intensity can reflect structural changes of the disc. Therefore, biochemical imaging techniques, in combination with a high-field strength MR scanner of a minimum of 3 T, may add a diagnostic value for the detection of lesions at an early stage. A widely used biochemical MR imaging technique is T2 mapping. This technique uses T2 relaxation times as an indirect indicator of structural changes in the cartilage collagen fiber organization and network. The interaction between water molecules and collagen fibers is used to visualize the collagen organization, extracellular matrix structure, and water content [6]. A change in T2 values can indicate early structural changes. The use of contrast agents is not necessary; thus, T2 mapping has been used in many studies of various joints, mostly for the evaluation of articular cartilage in patients with osteoarthritis and in patients after different cartilage repair surgery techniques, and in other tissues such as the intervertebral disc [7–13]. To the best of our
All experiments were performed in accordance with the ethical standards of the World Medical Association (Declaration of Helsinki). The approval of the ethics committee was obtained before the examination of the volunteers. All volunteers gave written, informed consent to use their anonymized data. Between October 2010 and July 2011, 14 volunteers were recruited. Twenty joints from ten volunteers were included in the study. Six volunteers were female, and four were male. The mean age (±standard deviation) was 26.1±6.6 years (range, 20 to 43). All volunteers underwent a clinical examination, including measurement of the mouth opening and palpation of the temporomandibular joint and muscles. Included were volunteers without pain, who had no mouthopening limitations, no clicking phenomena, and no anterior disc displacement in the temporomandibular joints. Exclusion criteria were age younger than 18 and older than 50 years; fixed orthodontic device; metallic foreign bodies in the head region; presence of biostimulators (pacemaker, insulin pump, etc.) and other contraindications to MR, such as claustrophobia, tremor, or other forms of motor unrest; and pregnancy. Two volunteers failed to appear for the MRI examination, one volunteer was excluded due to reciprocal clicking, and one volunteer had to be excluded because of anterior disc displacement without reduction. Magnetic resonance imaging MR imaging was performed on a 3-T MR scanner (Magnetom TIM Trio, Siemens Healthcare, Erlangen, Germany) using a flexible, dedicated, eight-channel multielement coil (Noras, Würzburg, Germany). For all volunteers, both joints were imaged simultaneously in the supine position with the mouth in the closed position (Fig. 1). In addition, images with the mouth in an opened position were obtained using standardized wedge blocks with a thickness of 25 mm. For the morphological evaluation of the disc position and rating of the perceptibility, we used oblique sagittal and oblique coronal slice orientations. MR sequences and imaging parameters are listed
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Fig. 1 Example of T2-weighted image (oblique sagittal, closed mouth) of the right TMJ of one volunteer
in Table 1. The technique used for T2 mapping of cartilage was a multiple spin-echo Carr–Purcell–Meiboom–Gill (CPMG) sequence [15, 16]. This sequence typically yields a series of T2-weighted images with variable echo times, which can be further post-processed into T2 maps.
sagittal and coronal slices in the opened and closed positions. All examiners assessed the images of the mouth in the closed position independently of each other, according to the perceptibility of position/delineation to surrounding tissue and morphology of the disc, using a five-point scale (1=excellent delineation with sharply defined border lines, 5=insufficient delineation, structures not circumscribable). The changes in the signal (evenly dark/central brightening/focal brightening/ disc residues) and morphology (biconcave/flattened/biconvex/deformed) of the disc were also evaluated [5]. The regions of interest (ROIs) for the T2 relaxation time maps were selected manually by each examiner. For the ROI of the TMJ disc, the contour of the disc and the anterior, central, and posterior part of the disc were drawn on the image that revealed the best morphological contrast and transferred via “copy and paste” into the T2 map (Fig. 2). To assess intraobserver reproducibility, these measurements were repeated after at least 4 weeks by the same investigator (M.S.), and to assess interobserver agreement, by the two other observers (M.B. and A.S.). The evaluation was performed at the Department of Radiology, under the supervision of a radiologist with 20 years of experience in clinical and experimental MR research and diagnostics.
Image analysis Statistical analysis Three experienced examiners who specialized in temporomandibular disease (TMD) therapy [M.S. (20 years experience), M.B. (more than 10 years of experience), and A.S. (more than 5 years of experience) in TMJ dysfunction syndrome treatment] were blinded to volunteer identity. One examiner (M.S.) assessed the normal location and position of the condyle and the disc on the morphological, oblique Table 1 MR measurement parameters for Carr–Purcell– Meiboom–Gill (CPMG), proton density (PD), and morphological dual-echo steady state (DESS) protocol
All statistical evaluations were performed using IBM SPSS Statistics version 19.0. Metric data, such as T2 values, are presented using mean ± SD. To assess the reproducibility of T2 evaluation, interobserver variability was calculated from three different evaluations in each region (ROIs 1–4) by three experienced independent raters. Results were expressed as CPMG Parasagittal (closed position)
DESS Coronal
PD Parasagittal (opened position)
FOV (mm × mm) Number of slices (left + right) Slice thickness (mm) Slice separation (mm) Number of averages TR (ms) TE (ms) Echo train
155×155 6+6 2 2.2 1 1,440 100.8 10
162×192 – 0.60 – 2 15.16 4.37 1
90×90 11+11 2 2.2 1 1,810 30 1
Total acquisition time (min/s) Acquisition matrix (pix) Percent phase field of view (%) Percent sampling (%) Pixel bandwidth (Hz/pix) MR acquisition type Reconstructed matrix (pix) Pixel spacing (mm)
14:47 384×384 100 100 200 2D 384×384 0.40×0.40
21:14 378×448 84.375 100 169 3D 756×896 0.21×0.21
4:56 384×384 100 100 161 2D 768×768 0.12×0.12
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Clin Oral Invest (2014) 18:1865–1871 Table 2 Summarized mean values ± std. deviation of ROI evaluations. ROI 1 includes the entire disc, ROI 2 includes the anterior part of the disc, ROI 3 includes the central part of the disc, and ROI 4 includes the posterior part of the disc. Each ROI was evaluated by three raters (left side, N =30; right side, N =30; both sides, N =60) Evaluator
Side
ROI
Mean
Std. deviation
No.
Total
Left
1
26.9
3.2
30
2 3 4 1 2 3 4 1 2 3 4
26.5 25.9 24.3 27.0 28.8 26.1 22.4 26.9 27.6 26.0 23.4
5.8 2.7 2.6 4.2 8.4 5.3 2.4 3.7 7.2 4.2 2.7
30 30 30 30 30 30 30 60 60 60 60
Right Fig. 2 Example of T2 map (oblique sagittal, closed mouth) of the TMJ of the selected volunteer shown in Fig. 1, with the ROIs delineated
intraclass correlation coefficients (ICCs). ICCs are based on all measurements per rater (one rater/ROIs 1–4, left/right side: N =80). In order to assess mean differences in T2 values between individual ROIs, a mixed model ANOVA was used, with an unstructured covariance matrix, taking into account multiple measures per volunteer. Bonferroni-corrected, pairwise post hoc comparisons were based on estimated marginal means. A value of p ≤0.05 was considered to indicate significant results.
Results All investigated joints demonstrated a normal condyle position and no anterior disc dislocation. Most of the discs showed normal signal intensity. Rater 1 diagnosed focal brightening of the disc in one volunteer (both sides), and rater 2 detected central brightening in one left joint and one right joint and focal brightening of the disc in one right joint. Rater 3 diagnosed one central brightening and one focal brightening in the right disc.
All joints
significant difference between raters (p =0.091) or sides (p = 0.810). When T2 values aggregated over both sides and the three raters were compared, post hoc tests revealed significant differences only between ROIs 1 and 4 (p =0.002).
Discussion Identifying possible predictors and risk factors for TMJ problems using MRI images remains a challenge. The risk of degenerative changes and joint effusion increases with displacement of the disc [17]. Joint effusion may be a predictor for the existence of synovitis [18–20]. Attempts have been made to correlate T2 signal values from T2-weighted images with symptoms of temporomandibular dysfunction. Sano and
Results of morphological assessment Mean values of a five-point scale (1=excellent to 5=very poor) for the perceptibility of position/delineation to surrounding tissue was (mean ± std. dev) 1.5±0.8 for the left side and 1.7±0.8 for the right side, and, for the morphology of the disc, 1.2±0.4 for the left side and 1.3±0.6 for the right side. Results of biochemical analysis (T2 relaxation time mapping) The mean values for the ROIs were between 22.4 and 28.8 ms, and the mean for all ROIs was 26.0±5.0 ms (Table 2). The ICC for interobserver variability was 0.698, and the ICC for intraobserver variability was 0.861. Figure 3 shows the results for all raters and ROIs. There was no statistically
Fig. 3 Mean T2 values for the different ROIs and the different raters. A clear tendency toward a decrease in T2 from the anterior to the posterior part of the disc is demonstrated
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Westesson found a correlation between TMJ pain and an increased T2-weighted signal in the retrodiscal tissue; however, no correlation between the T2 signal intensity and disc position could be found [21]. T2 mapping is regarded as a powerful technique that provides information about the status of the cartilage collagen network without the need for contrast agents [22]. This technique has been validated for the detection of collagen and may also be sensitive to proteoglycan, which was demonstrated in several studies investigating large joints, such as the knee [11, 22, 23]. The aim of this study was to evaluate whether T2 mapping of the articular disc of the temporomandibular joint is feasible and to assess the normal T2 relaxation time distribution within the TMJ to enable later patient studies using this biochemical technique. The presented work was intended as a “feasibility study.” Therefore, only ten asymptomatic volunteers (20 joints) were included in the study, and no power analyses were performed. The local ethics committee recommends ten cases, at most, for pilot (feasibility) studies. To the best of our knowledge, there are no reports in the literature about T2 mapping of the TMJ at 1.5 T. The signalto-noise ratio (SNR) of T2 mapping at 1.5 T is critical. Due to low SNR, the precision of the T2 values in the TMJ disc would be compromised, and this type of diagnostic technique would not be feasible. Several studies of the knee joints using T2 mapping at 1.5 T have been published [24–26]. The authors could find only one brief report dealing with T2 mapping of the TMJ [14]. Our study shows that T2 relaxation time measurements of the articular disc of the TMJ are feasible, with good inter- and intraobserver agreement. The highest T2 relaxation times were found in the anterior part of the articular disc, with lower T2 values in the central part of the disc, and the lowest values in the posterior part of the disc. As can be seen in histological specimens, in the anterior part of the disc, cross-sectioned collagen fiber bundles appeared thinner, and in the middle part, collagen fibers were more longitudinally sectioned and showed a more dense and organized orientation (Fig. 4). In contrast, the posterior part of the disc shows thicker collagen fiber bundles, mainly crosssectioned, strongly woven, and highly organized. Based on the histology, we can prove that the orientation of collagen fibers is not at the magic angle (54° 44′ relative to B0). Therefore, the magic angle effect, i.e., a local increase in the T2 relaxation time, is not observed in the TMJ disc. The MRI investigations were performed with the mouth in a closed position. It is possible that the decrease in values in the central, and particularly, in the posterior part, could have been caused by the greater pressure of the condyle in these regions. The interobserver agreement showed good reproducibility, with 0.7, and an intraobserver agreement greater than 0.8. The interclass agreement (0.8) for the whole disc was sufficient to reproducibly evaluate the T2 values of the disc. Figure 3 shows
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Fig. 4 Micromorphology of collagen fibers in the TMJ disc, using an undecalcified ground and polished section, after surface staining with Giemsa solution
a good inter-rater correlation for all ROIs, except for ROI 2 with rater 2. However, the absolute difference in T2 values was small and not statistically significant. The values for the central and posterior part of the disc showed a good intraclass correlation, with values greater than 0.8 and 0.7, respectively. It was surprising that ROI 2 did not differ from ROI 4, although the difference was larger than between ROIs 1 and 4. A possible reason may be that the variance in ROI 2 was larger than in any other ROI, indicating the most heterogeneous measurements within that ROI. A possible explanation for this is the morphology of the disc. The anterior part of the articular disc of the TMJ is usually larger than the central part and, in some cases, larger than the posterior part and thus shows a greater variety of T2 relaxation time values within the ROIs. Morphologically, the evaluated joints showed a normal condyle and disc position. The perceptibility of position/ delineation relative to surrounding tissue and of the morphology of the disc was rated as very good by all three raters. The limitation of the study is that only asymptomatic volunteers were enrolled. However, to assess the feasibility of T2 mapping in vivo and to become familiar with normal T2 relaxation time values in different regions of the healthy articular discs, a basic study with volunteers is necessary. Due to the limited number of volunteers in this study, more subjects should be studied to assess what is standard for the normal relaxation time distribution within the TMJ disc. Another limitation of the proposed technique is that it requires a high-field MR system operating at 3 T and a dedicated coil, which was available in the present study. The authors did not aim to bring this protocol into the clinic at the current stage. Therefore, a longer scan time was tolerated. In future studies, we will try to reduce measurement time in order to provide a clinically acceptable method. After further development, this method may be able to demonstrate lesions at a very early stage.
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The proposed T2 mapping technique with T2 relaxation time measurements enables an ultrastructural analysis of the composition of the articular disc of the TMJ. This biochemical technique is feasible in vivo, as shown in our study, when a high-field (3 T) MR and a dedicated TMJ coil is used, which provides sufficient signal-to-noise ratio to perform T2 mapping with reasonable resolution in a small structure like the TMJ disc. T2 mapping has the potential to provide additional information to standard morphological MR imaging, which may allow the diagnosis of early stages of disc degeneration before morphological changes occur. In addition, T2 mapping may be a sensitive tool for the monitoring of different therapies, both surgical and conservative, for various disorders of the TMJ. T2 mapping as a biochemical technique, together with morphological MRI, may help to gain more insights into the physiology and the pathophysiology of the articular disc in the TMJ, noninvasively, and in vivo. As a clinical diagnosis of TMJ is limited, MR, which can provide morphological and biochemical imaging, allows a more accurate analysis of TMJ disorders [2, 27–29].
Conclusion The T2 mapping technique enables ultrastructural analysis of the composition of the TMJ disc. This biochemical technique is feasible in vivo, as shown in our study, when a high-field (3 T) MR and a dedicated TMJ coil are used Acknowledgments This study was funded by the Austrian Science Fund FWF grant P23481-B19, Vienna Spots of Excellence of the Vienna Science and Technology Fund (WWTF), Vienna Advanced Imaging Center (VIACLIC FA102A0017), and grant VEGA 2/0013/14 of the Slovak Grant Agency. We would like to thank the volunteers, and we highly appreciate the technical support of Claudia Kronnerwetter. We would like to give a special thanks to Prof. Hanns Plenk from the Institute for Histology and Embryology/Medical University of Vienna and Prof. Monika Egerbacher from the Institute for Anatomy, Histology and Embryology of the University of Veterinary Medicine for their valuable support with the histological evaluation. Conflict of interest The authors declare that they have no conflict of interest.
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