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. Author manuscript; available in PMC: 2015 Apr 11.
Published in final edited form as: J Biomech. 2014 Feb 18;47(6):1360–1367. doi: 10.1016/j.jbiomech.2014.01.051

Functional Analysis of the Rabbit Temporomandibular Joint Using Dynamic Biplane Imaging

Sarah E Henderson 1, Riddhi Desai 1, Scott Tashman 1, Alejandro J Almarza 1,*
PMCID: PMC4010254  NIHMSID: NIHMS568290  PMID: 24594064

Abstract

The dynamic function of the rabbit temporomandibular joint (TMJ) was analyzed through non-invasive three-dimensional skeletal kinematics, providing essential knowledge for understanding normal joint motion. The objective of this study was to evaluate and determine repeatable measurements of rabbit TMJ kinematics. Maximal distances, as well as paths were traced and analyzed for the incisors and for the condyle-fossa relationship. From one rabbit to another, the rotations and translations of both the incisors and the condyle relative to the fossa contained multiple clear, repeatable patterns. The slope of the superior/inferior incisor distance with respect to the rotation about the transverse axis was repeatable to 0.14 mm/degree and the right/left incisor distance with respect to the rotation about the vertical axis was repeatable to 0.03 mm/degree. The slope of the superior/inferior condylar translation with respect to the rotational movement about the transverse axis showed a consistent relationship to within 0.05 mm/degree. The maximal translations of the incisors and condyles were also consistent within and between rabbits. With an understanding of the normal mechanics of the TMJ, kinematics can be used to compare and understand TMJ injury and degeneration models.

Keywords: temporomandibular joint, 3D joint kinematics

INTRODUCTION

Some estimates suggest that over ten million Americans are affected by temporomandibular joint (TMJ) disorders (TMDs) (NIH and NIDCR, 2010). Clinical symptoms of TMDs include jaw locking, clicking, headaches, joint pain and tenderness, restricted range of motion, painful mastication, and deterioration of the disc and the articulating surfaces of the TMJ (Wilkes, 1989). Clinical exams often used to diagnose TMDs only test the end positions of the teeth and do not focus on the travel path of the joint. It is important to understand the kinematics of the joint to determine if early changes in the function of the joint may suggest oncoming TMDs.

Knowledge of dynamic TMJ function through three-dimensional (3D) skeletal kinematics is essential for understanding normal joint behavior and investigating the effects of injury or disease in the TMJ. Many factors contribute to joint motion including muscular forces, passive structures constricting movement, and dynamic physical forces such as contact, gravity and inertia (Markolf et al., 1981; Schipplein and Andriacchi, 1991). However, little is known on how these factors combine for everyday movement, making replication of kinematics difficult (Tashman and Anderst, 2003). 3D visualization and measurement techniques are necessary to measure skeletal kinematics with high precision and accuracy.

Various kinematic studies have been performed on humans, many looking at the effects of partial and total joint replacement and other invasive treatments on joint motions (Baltali et al., 2008; Gallo, 2005; Keller et al., 2012; Leiggener et al., 2012; Linsen et al., 2012; Palla et al., 2003; Voiner et al., 2011; Yoon et al., 2007). While incisal movement alone is not enough to understand the movement of the mandibular condyles (Naeije, 2002; Travers et al., 2000), 3D jaw tracking systems have provided more insight into condylar motion (Baltali et al., 2008; Gallo, 2005; Keller et al., 2012; Leiggener et al., 2012; Linsen et al., 2012; Palla et al., 2003; Voiner et al., 2011). In-depth TMD patient studies have not been performed with these systems because it is hard to identify patients at early stages of dysfunction. The current 3D systems are beneficial for human patient studies, but cannot be implemented in non-compliant animal models.

Animal studies are uniquely suited for investigating the disease initiation and progression that cannot be completed and repeated in a patient study, by enabling both mechanical interventions that may drive disease development and comprehensive, invasive tissue assessment. In particular the rabbit model was chosen due to the various TMJ injury and degeneration models already established in the literature (Ali and Sharawy, 1995; Almarza et al., 2011; Axelsson et al., 1992; Chaves et al., 2002; Shaw and Molyneux, 1993; Timmis et al., 1986; Tominaga et al., 1999; Tominaga et al., 2000; Ueki et al., 2003). Rabbits also exhibit a grinding mastication similar to that of humans (Morita et al., 2008). Several studies have previously collected normal rabbit kinematics; however, most done were invasively and only focused on incisal movement (Huff et al., 2004; Inoue et al., 2004; Inoue et al., 1989; Langenbach et al., 2001; Morimoto et al., 1985; Schwartz et al., 1989; Tominaga et al., 2000; Weijs et al., 1989a; Weijs and Dantuma, 1980; Weijs et al., 1989b; Yamada and Haraguchi, 1995; Yamada et al., 1988; Yamada et al., 1990), instead of also understanding condylar movement (Morita et al., 2008).

Non-invasive 3D x-ray imaging systems have been developed to combine x-ray videos with 3D morphology from bone scans and have been extensively validated in human and animal joints (Bey et al., 2008; Bey et al., 2006; Brainerd et al., 2010; Tashman and Anderst, 2003; Tashman et al., 2007), including one study of normal minipig mastication (Brainerd et al., 2010). Our study investigated the dynamic nature of the TMJ condyle with respect to the fossa, as well as the incisor relationship in rabbits. The objective of this study was to determine and evaluate repeatable measurements of rabbit TMJ kinematics. The relative motion of the condyle with respect to the fossa was tracked. Maximal distances, as well as path, were traced and analyzed for the incisors and for the condyle-fossa relationship. By establishing kinematics for control animals, future kinematic assessments can be used to help understand the progression of specific TMDs.

METHODS

Animal Model

Three skeletally mature female New Zealand White rabbits, approximately 1 year in age, and weighing approximately 5kg, were purchased from Myrtle’s Rabbitry Incorporated (Thompsons Station, TN). All rabbits were examined by a veterinarian and were found to be in good health. All animal procedures were approved by the Institutional Animal Care and Use Committee at the University of Pittsburgh, in accordance with the National Institutes of Health guidelines for the use of laboratory animals.

Measurement of TMJ Kinematics: High-Speed Biplane Radiography

TMJ kinematics were assessed using a unique high-speed stereo-radiographic system, consisting of two sets of 110kW pulsed x-ray generators (CPX 3100CV; EMD Technologies, Quebec, Canada), 40cm image intensifiers (Thales, Neuilly-sur-Seine, France) using a 20cm field of view, and high-speed 4 Megapixel digital video cameras (Phantom v10, Vision Research, Wayne, New Jersey, USA). The system configuration is shown in Figure 1. Data was collected at a frame rate of at least 170 frames/s for 1s with 4 Megapixel image resolution. Short-duration (1ms) exposures were performed to acquire images free of motion blur.

Figure 1.

Figure 1

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High-speed biplane radiography was used for image collection. Rabbits were placed in a radiolucent box between two sets of x-ray generators and image intensifiers with high speed cameras.

This system has been used extensively for studies of joint motion in humans and animals, with accuracy in the range of 0.07–0.3mm for a 40cm field of view (Craig et al., 2008; Tashman and Anderst, 2003; Tashman et al., 2007). For these rabbit studies, a 20cm field of view was used, reducing image pixel size by a factor of two with a concomitant increase in accuracy.

The rabbits were placed in a ventilated radiolucent cage (Figure 1). Small pieces of dried fruit were placed in the rabbit’s mouth and radiographic images (Figure 2A) were acquired for a 1 second period. The process was repeated to collect at least three acquisitions per rabbit.

Figure 2.

Figure 2

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Sample x-ray image from the high resolution cameras at one frame in time (A). For 2D to 3D registration, the collected x-ray images (pink) are matched frame by frame with the virtual x-ray images (green) from the CT scan. One of the two combined images is shown for each the mandible (B) and the skull (C).

The model-based technique for determining 3D kinematics of skeletal structures from biplane radiographic views has been extensively described and validated. We have performed multiple in vivo and in vivo validations of our measurement methods for the knee, shoulder and cervical spine, by implanting beads on the bones (which can be tracked with high accuracy using well-established radio-stereometric techniques), and comparing this “gold standard" marker/bead tracking to the markerless tracking method employed for this study (Anderst et al., 2009; Bey et al., 2006; Haque et al., 2013; Tashman and Anderst, 2003; You et al., 2001). Typical 3D measurement precision for these studies is in the order of 0.1–0.2mm during dynamic testing (and substantially better than 0.1mm for static imaging). Dynamic accuracy for joint kinematics (relative motion between two bones) was measured directly, and was typically around ±0.5mm for translations and ±0.7degrees for rotations. These are direct assessments of accuracy for clinically relevant measurements acquired at functionally relevant movement speeds that account for propagation of all sources of error.

In actuality, the accuracy for this rabbit TMJ study was substantially better. Under similar bone sizes and imaging conditions, TMJ tracking accuracy would equal or exceed that for the knee/shoulder, because there are more features and image details in the skull and mandible than there are for the knee or shoulder. The knee and shoulder validation studies were done with radiographic imaging resolution of approximately 0.5mm/pixel and CT slice spacing of 0.6 or 1.2mm (within-slice resolution of approximately 0.5mm). The rabbit jaw is much smaller, so a smaller field of view was employed; the images used for tracking had a pixel size of approximately 0.125mm. Head/jaw CT scans were obtained using a micro-CT system with isotropic, 0.1mm voxels. While we have not specifically assessed accuracy under these conditions, it is certain that better imaging resolution will improve tracking accuracy. We are conservatively estimating that this 400% improvement in radiographic image resolution, combined with a 500% (or better) improvement in CT scan resolution (along with the greater bone details inherent in the skull and mandible images), will result in a error reduction (relative to the shoulder/knee studies) of at least a factor of 2. Thus, we estimate that the accuracy for TMJ kinematics is approximately ±0.2mm in translation and ±0.4degrees in rotation. For the incisors, this 0.2mm error relates to 5% error in the differences in superior-inferior translations measured between rabbits. For the condyles, an error of 0.2mm results in a 15% error in the differences in superior-inferior translations measured between rabbits.

Briefly, a 3D model of each bone to be tracked was derived from a computed tomography (CT) scan (as described below). A virtual model of the biplane x-ray system was created for generating a pair of digitally reconstructed radiographs (DRR’s) via ray-traced projection through the CT bone model. The bone model was automatically repositioned within the virtual model until a best match was achieved between the simulated DRR’s and the actual radiographic image pair (Figure 2B,C). This technique determined the 3D positions and orientations of the mandible and the skull for each motion frame.

Bone Models from Micro-Computed Tomography

Accurate, animal-specific bone models were required for both model-based tracking and kinematic analysis. After euthanasia, the entire head, including the mandible and skull, was scanned at high resolution (102.5µm isotropic voxels) using a micro-computed tomography system (Inveon micro-CT system by Siemens at the Rangos Research Center Animal Imaging Core, Children’s Hospital of Pittsburgh of UPMC). The mandible and skull bones (with teeth) were segmented from each other and from soft tissue and reconstructed into both surface and volumetric models using Mimics software (Materialise, Inc).

Coordinate Systems

Anatomical coordinate systems were set up similar to the systems used by Brainerd et al. (Brainerd et al., 2010). The transverse axis was aligned through the center of the condyles (or fossas for the skull), the longitudinal axis was parallel to the occlusal plane (where the molars meet) running posterior to anterior, and the vertical axis was the cross product of the transverse and longitudinal axes (Figure 3). The coordinate systems were centered between the condyles and fossas for the mandible and skull, respectively. The orientations of the anatomical coordinate systems were determined using standard rigid body transformations, and translations and rotations were determined. The joint rotations were calculated in the order of rotation about the transverse axis, rotation about the vertical axis, and rotation about the longitudinal axis.

Figure 3.

Figure 3

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The anatomical coordinate system for the mandible (A) was set up with the transverse axis (x-red) was aligned through the center of the condyles, the longitudinal axis (y-green) was parallel to a plane through the occlusal plane (where the teeth meet), and the vertical axis (z-blue) was the cross product of the transverse and longitudinal axes. The skull coordinate system was set up in a similar manner (B). The coordinate systems were centered between the condyles and fossas, for the mandible and skull respectively.

Analysis of Biodynamics

Our analysis focused on the dynamic behavior of the TMJ rather than only the end of range displacement of the jaw. The center points on the incisors were tracked in all three planes (Figure 4A,B). The relative motion of the condyle in relation to the fossa was tracked by placing points at the most superior point of the condyle and in the concave region of the fossa (Figure 4E,F). The relative motion of the centers of the two points was determined in all three anatomic planes. These points were rigidly fixed and the position measured in each frame. A future study will need to determine the reliability of determining the coordinate planes.

Figure 4.

Figure 4

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Points placed for measurements. (A) Mandible incisor point, superior view (B) Skull incisor point, anterior view. (C) Vector demonstrating the distance between the incisor points. (E) Condylar point, anterior view. (F) Fossa point, inferior view. (G) Vector indicating the distance between the condylar point and the fossa point (condyle is labeled with C and the fossa with F). Figures are labeled by directions: A-anterior, P-posterior, M-medial, L-lateral, S-superior, I-inferior.

For each animal, kinematics from at least three representative chewing cycles were analyzed from each of a minimum of three different acquisitions. Three acquisitions per rabbit were chosen based on the observation of three distinctive complete chewing cycles; one chewing cycle is equal to a full opening and closing of the mandible. One full chew cycle was determined on a time graph to be the distance or rotation from one peak to the next peak (Figure 5). Analyses were performed to determine the maximal translations and travel paths for both the incisors and the condyles.

Figure 5.

Figure 5

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A.) The change in distance of the mandible incisors from the skull incisors with relation to time. B.) The change in the rotation of the mandible around the vertical, transverse and longitudinal axes with relation to time. One chew cycle is considered to be from one peak to the adjacent peak. Representative data shown.

Incisors-Maximal Translations

Motion of the incisors was described by quantification of their total displacement right/left, superior/inferior, and anterior/posterior during a chew cycle from peak displacements in each direction during each chew cycle (Figure 5A). Thus, three parameters of the contact point on the incisors were compared: 1) Maximal change in superior/inferior translation; 2) Maximum left/right translation; 3) Maximum anterior/posterior translation.

Incisors-Path

To describe path, each mandible rotation in the coordinate plane (Figure 5B) was compared to each incisor translation to identify any relationships that existed. The translation-rotation relationships analyzed were chosen when a repeatable linear pattern was observed, which allowed for the slope to be compared between different acquisitions. If no repeatable and/or linear pattern was observed, the slope was not calculated. The following slopes were chosen for analysis: 4) Slope of the superior/inferior translation of the incisors with respect to mandible rotation about the transverse axis (Figure 6A); 5) Slope of the left/right translation of the incisors with respect to the mandible rotation about the vertical axis (Figure 6B).

Figure 6.

Figure 6

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Comparison of the distance of the mandible incisors from the skull incisors with respect to the rotation of the mandible. (A.) The distance traveled superior/inferior with respect to the rotation of the mandible around the transverse axis. (B.) The distance traveled right/left with respect to the rotation of the mandible around vertical axis. Representative data shown.

Condyle-Maximal Translations

The movement of the mandible was somewhat elliptical in the coronal plane and always started to the same side during an acquisition. As established in the literature, the side in which the mandible first moves is the working side, while the other is called the balancing side (Morita et al., 2008). The total displacement for both the working side and balancing side condyles was measured. Total superior/inferior displacement was found by subtracting the maximal opening from the maximal closing of the mandible relative to the fossa during a chew cycle. Additionally, the total displacement anterior/posterior was calculated. The left to right condyalr displacement was minimal. The following parameters were described: 6) Maximum working condyle superior/inferior translation relative to the fossa; 7) Maximum balancing condyle superior/inferior translation relative to the fossa; 8) Maximum working condyle anterior/posterior translation relative to the fossa; 9) Maximum balancing condyle anterior/posterior translation relative to the fossa.

Condyles-Path

The translations of the condyles were plotted with respect to the mandible rotations, and the relationships to be analyzed were chosen when a repeatable linear pattern was observed, which allowed for the slope to be compared between different acquisitions. If no repeatable and/or linear pattern was observed, that specific evaluation was not used. The analysis of the superior/inferior movement of the condyle relative to the fossa with respect to the rotation of the mandible about the transverse axis was performed according to the direction of chewing. Analysis depended on the side of mastication as well as the opening and closing of the mouth. The only repeatable behavior was seen in the superior/inferior translation of the condyles with respect to the transverse axis rotation of the mandible (Figure 7A,B). For this measure, a linear pattern was observed when analyzing the slope of only the first fifty percent of the closing cycle. Comparisons were made amongst the slopes calculated from the closing condyle cycle of the working and balancing sides of the mandible: 10) Slope of the working side superior/inferior translation of the condyle relative to the fossa with respect to the mandible rotation about the transverse axis; 11) Slope of the balancing side superior/inferior translation of the condyle relative to the fossa with respect to the mandible rotation about the transverse axis.

Figure 7.

Figure 7

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Comparison of the distance of the condyle relative to the fossa with respect to the rotation of the mandible. The distance traveled superior/inferior with respect to the rotation of the mandible around the transverse axis of the working side condyle (A.) and the balancing condyle (B.). At an angle of 0° the mouth is considered to be closed. The opening of the mouth translations are represented by the bottom line of the ellipse and the closing of the mouth translations are represented by the top line. Representative data shown.

Statistical Analysis

In summary, first, to determine differences amongst chewing stage (opening and closing) for all biodynamics parameters for multiple chewing cycles a student t-test was performed. The data was found to have a normal distribution using the Anderson-Darling Test for Normality. Then, a one-way ANOVA (Minitab 16, State College, Pennsylvania, USA) with Tukey’s post hoc testing was then used to assess differences for all biodynamics parameters amongst chewing cycles within individual acquisitions, amongst acquisitions within each rabbits, and amongst rabbits from at least three acquisitions. The data used for the ANOVAs was found to have a normal distribution using the Anderson-Darling Test for Normality. A statistically significant difference was established as p<0.05. All data was reported as an average±standard deviation of the mean.

In more detail, statistical analyses for all reported biodynamic variables were performed in four stages. Firstly, chewing stage (opening, closing) within a chewing cycle, for all chewing cycles, acquisitions, and rabbits were assumed to be different; however, no statistical significances were found and therefore the values for opening and closing for each chew cycle were averaged into one opening/closing value per cycle. Then secondly, all chewing cycles (at least three) within an acquisition, for all acquisitions and rabbits were assumed to be different; however, no statistical significance was found for the opening/closing value between chew cycles and hence the values of chew cycles for each acquisition were averaged into one chew cycle value per acquisition. Thirdly, acquisitions (at least three) for each rabbit, for all rabbits were assumed to be different; again, no statistically significant differences were observed. Thus, all biodynamic parameters are averaged into one acquisition value per rabbit. Fourthly, acquisitions between rabbits were assumed to be different; and in this case one rabbit was different than the other two, which did not allow for the data to be averaged for all rabbits.

RESULTS

Evaluation of the movement of the upper and lower incisors from opening to closing revealed a periodic pattern in all three directions and all three rotations (Figure 5). In the superior/inferior direction, the total incisor displacement was 9.03±1.55mm for Rabbit 2, which was statistically different from the other two rabbits with an average displacement of 14.55±3.71mm (p<0.05, for details see Table 1). The total displacement, between the upper and lower incisors in the right/left direction was statistically different for Rabbit 2 with a distance of 3.70±1.11mm compared to the average of other two rabbits at 6.58±1.09mm (p<0.05, Table 1). In the anterior/posterior direction, the maximum displacement was significantly different between Rabbits 1 (4.99±1.13mm) and 2 (1.82±0.43mm), but neither were different from Rabbit 3 (3.20±0.86mm) (p<0.05, Table 1).

Table 1.

Kinematic data sorted by consistent and variable measurements across rabbits including: total incisor displacements, slopes of incisor displacement with respect to rotations, total condyle displacement and slope of condyle displacements with respect to rotations for the working and balancing condyles. The average and standard deviation values are presented. Values are significant when p<0.05.

Rabbit 1 Rabbit 2 Rabbit 3
Consistent Measurements
Slope of Incisor Distance Right/Left vs. Vertical Rotation −1.39 ±0.07 −1.42 ±0.08 −1.39 ±0.01
Total Working Condyle Displacement Anterior/Posterior 5.24 ±0.73 3.20 ±1.63 4.94 ±0.36
Total Balancing Condyle Displacement Anterior/Posterior 4.35 ±0.49 3.50 ±0.05 4.18 ±0.18
Slope of Working Condyle Distance Superior/Inferior vs. Transverse Rotation 0.23 ±0.04 0.21 ±0.02 0.18 ±0.01
Variable Measurements
Total Incisor Displacement Superior/Inferior 16.52 ±2.12 9.03 ±1.55* 12.59 ±4.28
Total Incisor Displacement Right/Left 7.03 ±0.70 3.70 ±1.11* 5.90 ±1.51
Total Incisor Displacement Anterior/Posterior 4.99 ±1.13^ 1.82 ±0.43^ 3.20 ±0.86
Slope of Incisor Distance Superior/Inferior vs. Transverse Rotation 1.18 ±0.03 1.33 ±0.04* 1.21 ±0.01
Total Working Condyle Displacement Superior/Inferior 2.42 ±0.18* 1.46 ±0.16 1.72 ±0.31
Total Balancing Condyle Displacement Superior/Inferior 1.95 ±0.18* 1.50 ±0.05 1.36 ±0.01
Slope of Balancing Condyle Distance Superior/Inferior vs. Transverse Rotation 0.10 ±0.01 0.14 ±0.01* 0.07 ±0.01
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*

p<0.05 when different from other two rabbits

^

p<0.05 between rabbits with ^ but not with the third rabbit

Repeatable measurable relationships (Figure 6) were found by determining the slopes of the incisor displacement in the superior/inferior direction with respect to the rotation of the mandible about the transverse axis curves. Rabbit 2 (1.33±0.04mm/degree) was statistically different from Rabbits 1 and 3 (1.19±0.03mm/degree) for the slope of the superior/inferior displacement with respect to rotation about the transverse axis (p<0.05). The slopes of the incisor displacement right/left with respect to the rotation of the mandible about the vertical axis curves were also repeatable with an average of −1.38±0.06mm/degree with no statistical differences between rabbits (p<0.05, Table 1).

Comparison of the distance of the condyles of the mandible from the fossas in the superior/inferior, right/left, and anterior/posterior directions with respect to the rotation around the transverse axis, longitudinal axis, and vertical axis showed various discernible patterns. The superior/inferior displacement of the working condyle showed that Rabbit 2 and 3 had an average displacement of 1.59±0.25mm where as Rabbit 1 had a statistically different total displacement of 2.42±0.18mm (Table 1). Similarly, an analysis for displacement superior/inferior of the balancing condyle showed that Rabbit 2 and 3 had an average displacement of 1.43±0.09mm where as Rabbit 1 had a significantly different displacement of 1.95±0.18mm (Table 1). Between rabbits, the average working condyle displacement anterior/posterior was 4.57±1.24mm and the average balancing condyle displacement anterior/posterior was 4.07±0.48mm (Table 1). Neither parameter showed statistically significant differences amongst the rabbits. The right/left condylar displacement was generally less than 0.5mm and did not follow a consistent pattern and was not compared.

The relationship between the distance superior/inferior with respect to the rotation around the transverse axis of the condyle relative to the fossa created a repeatable pattern for both the chewing and balancing condyle (Figure 7). All other relationships showed neither a linear nor consistent repeatable pattern. Within rabbits, the slope of the closing cycle of the working condyle slope averaged was 0.21±0.04mm/degree with no statistical differences between rabbits (Table 1). The closing cycle of the balancing condyle slope was 0.14±0.01mm/degree for Rabbit 2, which was statistically different from the other two rabbits with a value of 0.09±0.02mm/degree (p<0.05). The slope of the condyle on the working side as the mouth closed was roughly two times larger than the slope of the condyle on the balancing side (p<0.05).

DISCUSSION

The characterization of the kinematic masticatory patterns of the rabbit is important in understanding the normal movement of the TMJ. The normal mechanics of the TMJ can be used to compare and distinguish kinematics of injured/degenerated joints, as well as healing joints. Our results demonstrate that from one rabbit to another the rotation and translation of both the incisors and the condyle movement relative to the fossa contain many clear, repeatable patterns. Specifically, for the incisors, the slope of the superior/inferior distance with respect to the rotation about transverse axis was repeatable to 0.14mm/degree and the right/left distance with respect to the rotation about the vertical axis was repeatable to 0.03mm/degree. For the condyles the slope of the superior/inferior translation with respect to the rotational movement about the transverse axis showed a consistent relationship within trials of each rabbits and between all of the rabbits to within 0.05mm/degree. Furthermore, the maximal translations of the incisors and condyles were also consistent within rabbits and between rabbits. Some differences between the individual rabbits were expected, due to the natural variations between rabbits.

Previous studies have used various methods of recording rabbit jaw kinematics including magnetic sensing systems, photoelectric sensing systems, cineradiographic systems and video recording systems (Huff et al., 2004; Inoue et al., 2004; Inoue et al., 1989; Langenbach et al., 2001; Morimoto et al., 1985; Morita et al., 2008; Schwartz et al., 1989; Tominaga et al., 2000; Weijs et al., 1989a; Weijs and Dantuma, 1980; Weijs et al., 1989b; Yamada and Haraguchi, 1995; Yamada et al., 1988; Yamada et al., 1990). These studies were all invasive with the placement of bone markers, sensors, magnets, and screws. Comparing our results to previous rabbit kinematic studies showed that our study yielded similar findings. In several studies, the chewing patterns were studied by affixing a magnet to the mandible and a magnetic sensor to the skull and the voltage differences were measured (Inoue et al., 2004; Langenbach et al., 2001; Morita et al., 2008; Tominaga et al., 2000; Yamada and Haraguchi, 1995; Yamada et al., 1988; Yamada et al., 1990). The general paths and patterns of the incisors in the vertical and horizontal directions were similar to what we observed (Figure 8), but numerical comparison was not possible, due to the measurement techniques. Similar chewing patterns were also seen with the photoelectric sensing systems (Inoue et al., 1989; Morimoto et al., 1985; Schwartz et al., 1989). The cineradiographic studies allowed for comparisons of the rotations about the transverse axis, similar rotations were found generally ranging from approximately 10–14° (Weijs et al., 1989a; Weijs and Dantuma, 1980; Weijs et al., 1989b). Another study found similar results for the incisal movement as rabbit study using 3D video analysis with skin markers during mastication of food and water (Huff et al., 2004). The superior/inferior displacement with food was roughly 13.1±3.0mm compared to our average between the three rabbits being 12.7±3.7mm. However, unlike our results the right/left movement recorded was larger with a mean of 17.6±3.0mm as opposed to our mean of 5.54±1.70mm, which was closer to their mean for the water stimulus (3.6±0.5mm) (Huff et al., 2004). The difference may arise from the variability that arises from the use of skin markers and the type of food stimulus.

Figure 8.

Figure 8

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Translation of the mandible incisors from the skull incisors in the coronal plane. The total movement superior/inferior with respect to right/left for three chewing cycles within one acquisition of one rabbit. Representative data shown.

One rabbit research study measured the mandibular condylar movement during mastication (Morita et al., 2008). The measurements were invasively done by removing the zygomatic arch and recording the motion of the condyles with a video camera on anaesthetized rabbits. Similar working side and balancing side path patterns for the motion of the condyles to our paths (Figure 9) were found. The incisor paths were also similar and recorded by magnetic sensors.

Figure 9.

Figure 9

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Condyle Distance - Translation of the condyle relative to the fossas in the sagittal plane. (A.) Total movement of the working side condyle superior/inferior with respect to right/left and (B.) total movement of the balancing side condyle superior/inferior with respect to right/left. The translations shown are for three continuous chewing cycles within one acquisition of one rabbit. Representative data shown.

The dynamic biplane x-ray imaging system we used was beneficial because it allowed for non-invasive measurement of normal rabbit chewing, both at the incisors and within the joint space. In the future, our system can be used to determine kinematic differences and changes over time in chewing patterns between healthy and degenerated joints in animal models. Gaining a better understanding of the current models used for TMD and the fibrocartilage degeneration process, will allow for development of more appropriate models to better understand TMDs. Based on evidence that TMJ degeneration and pain results in alterations in oral-motor patterns, we hypothesize that kinematic analysis will identify a specific pattern of use-dependent changes in joint function that constitute a signature for the presence of permanent degeneration and pain. This will be studied in the future through the use of a mechanical induction of TMJ degeneration using unilateral dental splints.

ACKNOWLEDGEMENTS

We would like to acknowledge Amy McCarty for her help with rabbit training and model based tracking. We would like acknowledge funding from the National Science Foundation under grant number 0812348, as well as from the National Institutes of Health under grant number T32 EB003392-01, The University of Pittsburgh Research Fund, and the University Of Pittsburgh School Of Dental Medicine.

Footnotes

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Conflict of Interest Statement

The authors have no conflicts of interest to disclose.

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