MotivationBackground Videofluoroscopic Swallow Studies (VFSS) are an accepted gold-standard for evaluation of swallowing function and an important tool for the diagnosis of dysphagia. The images ob-tained have contrast due to attenuation of the X-ray beam as it passes through the subject. The result is a 2D sagittal projection of the patient with contrast due primarily to bone and very little soft tissue contrast. Food and liquids are doped with Barium to allow visualization of the bolus. With certain cases, exposure to ionizing radiation can be a concern because the X-ray beam must be on continuously during the Video-fluoroscopic examination. Videofluoroscopy regularly achieves at least 30 frames per second (FPS) while maintaining a high signal to noise ratio (SNR). In contrast, magnetic resonance imaging (MRI) can provide excellent soft tissue contrast from restrict-ed planes, “slices,” of tissue at arbitrary orientations with arbitrary slice thickness. Whereas VFSS relies on a Barium-doped bolus to outline soft tissue structures, MRI can visualize soft tissue structures directly, re-gardless of bolus position and without contrast agents, e.g., during a dry swallow.

Weaknesses One of the main deficiencies of MRI in swallowing examination has been speed. Many previous MRI studies (Hartl et al., 2003; 2006) captured an image in ~700ms, meaning only about 1-2 images per normal swallow. Another study (Schipper et al., 1994) has improved speed by splitting each image acquisition across several “gated” repetitions of the swallowing motion, which improves tempo-ral resolution but introduces blurring due to variation across swallows. The “gated” method acquires part of each image during each repetition of a swallow. The downside is that any variability in the swallow causes blurring in the final images which represent an average swallow. An un-gated method collects images with regular temporal spacing while the subject swallows freely. Another challenge faced by MRI in this ap-plication are the many air-tissue interfaces of the nose, mouth, and throat. MRI relies on a strong and ex-tremely homogenous main magnetic field in the region to be imaged. Differences in magnetic susceptibil-ity between air cavities and tissue cause inhomogeneity in the main magnetic field which can cause signal loss, blurring, and geometric distortion.

Improvements Our work has focused on improving temporal resolution and correcting dis-tortion due to air-tissue interfaces. We have developed a custom MRI pulse sequence optimized for fast, sequential (un-gated) imaging of the oropharyngeal area as well as post-processing tools for susceptibility correction and accurate timecode generation.

MethodsScanner Imaging scans were performed on a Siemens Magnetom Allegra 3 T head-only scan-ner in accordance with an approved Institutional Research Board protocol. The Allegra offers a high-per-formance gradient set with a maximum gradient strength of 40 mT/m and a maximum slew rate of 400 mT/m/ms. Images were acquired with a single channel birdcage head coil.

Sequence A customized multi-shot spiral FLASH sequence was used with a reduced field of view technique. Tissues outside of the field of view were saturated using two orthogonal regional satura-tion pulses during the scan.

Parameters Midsagittal images were collected with 5.2 ms TR, 0.9 ms TE, flip angle 7°, 8mm slice thickness, 120x120mm FOV, 64x64 matrix, 6-shot spiral design, and repeated either 250 or 400 times for scan durations of 11.02 or 17.63 seconds. Regional saturation pulses were 120mm wide and placed so that they saturated spins superior to the hard palate and posterior to the posterior pharyngeal wall.

Timings Our sequence achieved a native frame rate of 22.7 FPS, or an image every 44.1ms. Each image is reconstructed from 6 consecutively acquired interleaves. The temporal blur of each image, 23.9ms, is the time between the start of the first interleaf ’s readout and the end of the last interleaf ’s read-out. Images are acquired in the order they will be displayed from a single swallowing event. In contrast to sequences requiring retrospective reorganization, where different phases of a swallow are collected across repeated swallows, our method allows accurate knowledge of the time between swallowing images like the timecode generator commonly used in VFSS.

Experiments Several 10-20 second scans were collected with a single subject swallowing dif-ferent types of boluses in the supine position. The subject was a healthy young adult with no history of swallowing disorder. In separate scans the subject dry swallowed, drank water from a straw, swallowed pudding, and chewed and swallowed a cookie. Pudding was chosen because its short T1 value, as mea-sured by Goehde et al. (2004), resulting in enhanced contrast in our images. Cookie was chosen to allow visualization of mastication and swallowing of a solid bolus.

Trade-Offs

The Compromise To achieve clinically relevant imaging speed with sequential image cap-ture requires that the readout of image data occur as fast as possible and with minimum overhead. This design goal inspired the use of the simpler gradient echo method as opposed to a spin echo sequence like in Hartl et al. (2006). Gradient echoes can be executed more quickly and with less RF power deposition but lack the spin echo’s ability to negate the effects of magnetic field inhomogeneity such as that from magnetic susceptibility. Because we use gradient echoes, longer readouts incur greater amounts of geomet-ric distortion due to the many air-tissue boundaries in the mouth and throat. To counter that, image data are collected across several shorter readouts in individual interleaves. However, each interleaf brings with it another excitation pulse and spoiler, adding overhead and reducing frame rate.

Balancing Goals Soft palate elevation, occurring on the order of 100ms (Kuehn, 1976), was the basis for our target frame rate. To capture more than two frames during the elevation requires greater than 20 FPS. Magnetic field maps, showing inhomogeneity due to magnetic susceptibility, indicat-ed distortion in the range of 300 Hz. Our goal then is a bandwidth per pixel (BWPP) of greater than 300 Hz to limit distortion and blurring to less than a 1 pixel radius. From the results of simulation in Figure 1, we determined that a spiral design with 6 interleaves per image was the only choice that met both our cri-teria for frame rate and distortion.

Sequential Prospective AcquisitionSequential vs. Gated Sequential imaging captures each image in its entirety as fast as possible during a swallow. Gated imaging collects segments of an image over repeated swallows. Although gated methods can improve frame rate or resolu-tion by simply extending the number of repetitions, they also suffer from increased blurring due to the variability between repeated swallows. Although sequential imaging is greatly limited in terms of contrast options and resolution by the need to collect an entire image’s worth of data as fast as possible, we chose it for the ability to evaluate highly variable motions without the need for repeti-tion.

Prospective vs. Retrospective Ordering Retrospective ordering methods, such as in Hartl et al. (2006), capture only a couple images per swallow from a series of swallows. Because the image capture interval is not aligned with the volitional swallowing, different phases of the swallow are captured out of order. Retrospectively the ensemble of images are re-arranged to place the swallowing phases in order and form a pseudo-movie of the swallowing process (collected from several swallowing events). Although variability between swallows does not cause blurring, it may corrupt analysis of swallowing function. Additionally, there is no information about the relative timing between reordered frames, making it impossible to extract temporal measures such as oral transit time (OTT), pharyngeal transit time (PTT), or delay in the triggering of swallow. Our sequential pro-spective method, however, captures images in the same order, and at the same rate at which they should be played back. This enables accurate timing of events occurring within a single swallow.

Magnetic SusceptibilityEffect on Image Quality Differences in magnetic susceptibility between tissue and air spaces can distort the local magnetic field around air-tissue interfaces. Localization of MRI signal relies on the assumption that the main magnetic field is homogenous. Field inhomogeneity can cause spurious phase accumulation resulting in geometric distortion or blurring in the image. Field inhomogeneity can also dephase spins within voxels, causing signal loss and dark voids in the image.

Controlling Factors The magnetic field inhomogeneity at air-tissue interfaces is a property of the main mag-net’s field strength, the material properties of the air and tissue, and the shimming of the scan volume. There are several sequence design options available to mitigate the effect of that inhomogeneity. By shortening the echo time (TE), spins have less time to accumulate spurious phase due to the inhomogeneity, resulting in less signal loss. Shortening the readout duration similarly lim-its the accumulation of spurious phase during data acquisition, resulting in less image distortion. For this reason, spiral readouts are commonly broken into “shots”, or “interleaves”, so that during each interleaf no significant phase accumulation occurs. Finally, various methods of post-processing use a map of the magnetic field inhomogeneity (obtained separately or extracted from the im-age itself ) to attempt to undo the phase accumulation.

Moving Window ReconstructionMulti-shot Imaging To avoid distortion and signal loss due to magnetic susceptibil-ity our sequence splits each image acquisition into 6 sequential interleaves. Each interleaf is prefaced by a slice-selective RF pulse followed by readout and a spoiler. Between every image (group of 6 shots) the regional saturation pulses are run to continue to exclude signal from regions outside of our field of view. Regular reconstruction creates images from each set of 6 interleaves separated by the regional saturation pulses (FPS 22.7). Moving window (MW) reconstruction creates additional images from sets of inter-leaves across the regional saturation pulse boundaries. The number of interleaves in common between MW images determines the enhancement of frame rate.

Advantage Over Interpolation Interpolation can also be used to increase frame rate, generating more frames between the ones actually measured. Unlike MW reconstruction, which re-groups collections of interleaves to generate new frames, interpolation works on reconstructed images. The images, which already contain a 44.1ms temporal blur, are then blended together by an interpolator resulting in 88.2ms temporal blur. Although the majority of MW images have increased temporal blur due to regional saturation pulses occurring within interleaf collections, the temporal blur is still less than interpolation.

ResultsAnatomical Observations MRI visualization was limited, in most subjects, to the oral and pharyngeal cavities. Anatomy which was very clearly visualized were the tongue, hard palate, soft palate, nasopharynx, oropharynx, and posterior pharyngeal wall (Figure 4). The lips, mandible, hypopharynx, and epiglottis were included in the field of view but less clearly resolved due to signal loss or receiver coil inhomogeneity. One important distinction from VFSS is that image data comes only from an 8mm thick midsagittal slice as opposed to a lateral projection of all of the anatomy of the head. Therefore, the MRI image allows a clear view of soft tissue structures, which in VFSS are obstructed by the higher contrast of overlapping bone in the mandible and skull.

Speed Without moving window reconstruction our sequence achieved 22.7 frames per second, or an image every 44.1ms. Because motion blur is only ac-cumulated during data acquisition; temporal blur, the time from the beginning of the first readout till the end of the last interleaf ’s readout, is 29.3ms. The dry swallow scan collected 250 images in 11.02 seconds while all other scans collected 400 images in 17.63 seconds. Moving window reconstruction, with a target frame rate of 30 FPS, achieved 33.3±5.4ms frame spacing with a temporal blur of 38.5±5.8ms. The step size for the window was 4.53±0.7 interleaves meaning that, on average, only 24.5% of information was shared between consecutive frames.

Physiological Observations In our swallowing trials we were able to visualize many of the physiological processes of the oral and pha-ryngeal stages of swallowing. Mastication could be observed without motion artifact due to the high frame rate achieved and resilience of spiral design sequences to motion. Suction during straw drinking could be observed (Figure 7). Bolus formation and oral transport stages could also be clearly visualized (Figures 6, 8). Soft palate visualization was extremely clear, allowing visualization of oropharyngeal closure during bolus formation and suction as well as nasopharyngeal closure during swallow (Figure 5). Bolus propulsion through the oropharynx is well captured, including posterior movement of the base of the tongue (Figures 5, 6, 8). In the cookie swallow data set, formation of Passavant’s Cushion could be seen during nasopharyngeal closure (Figure 5).

Technical Observations As a result of the extremely short echo time and repetition time, our images displayed little contrast, but predomi-nantly related to T1. Image noise was high due to the high bandwidth of the fast acquisition and the small flip angle of (7°), necessitated by the short TR. No significant aliasing pattern was observable in our reduced field of view, indicating good suppression of signal from the outer volume. The bright contrast observed from the water bolus was surprising (Figures 7,8) because water’s long T1 relaxation time should cause it to show up dark due to our short repetition time (TR). Chocolate pudding, which was measured by Goehde et al. (2004) as having a short T1 relaxation time, showed up with high signal intensity as expected (Figure 6). Neither dry swallow or cookie swallow boluses provided positive contrast in our images (Figure 5).

DiscussionSummary In this work we have demonstrated an improvement to raw imaging speed, and the ability to image at clinically relevant rates with an unob-structed view of soft tissue structures in the oral and pharyngeal cavities. Additionally, our method can provide accurate and precise timings for each frame, like a timecode generator in VFSS, allowing measurements of the durations of swallowing phases. We also demonstrated that simple foods such as water and pudding can provide dramatic positive contrast without doping with contrast agents such as Gadolinium. Our results illustrate the ability of MRI to visualize anatomy and physiology critical to the process of swallowing without exposure to ionizing radiation.

Future Work In order to serve as a general purpose tool for swallowing evaluation, the field of view must be extended to include the larynx, hypophar-ynx, and upper esophageal sphincter (UES). This limitation could be addressed by application of this sequence to a full-body MRI scanner with additional RF coils covering the neck. Improvements to the suppression of signal from areas surrounding the reduced field of view could enable improved frame rate or reduce aliasing artifact. Other methods, such as steady state free precession (SSFP), may improve image contrast and reduce noise by preserving signal between excita-tions, however the field inhomogeneity imposes a high bandwidth constraint that may not be feasible at 3 T. Application of compressed sensing techniques may allow for improvement to image resolution, field of view, or frame rate.http://mrfil.bioen.uiuc.edu/shared/drs2008/

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Figure 5. Cookie Swallow: Oral transport phase A selection of consecutive frames with 44.1ms spacing

Figure 6. Chocolate Pudding Swallow: Oral transport phase A selection of consecutive frames with 44.1ms spacing

Figure 7. Straw-drinking Water: Suction, Oral preparatory phase A selection showing every other frame with 88.2ms spacing

Figure 8. Straw-drinking Water: Oral transport phase A selection of consecutive frames with 44.1ms spacingReduced FOV

References Goehde et al.. Impact of diet on stool signal in dark lumen magnetic resonance colonography. Journal of magnetic resonance imaging

(2004) vol. 20 (2) pp. 272-8Hartl et al.. Cine magnetic resonance imaging with single-shot fast spin echo for evaluation of dysphagia and aspiration. Dysphagia

(2006) vol. 21 (3) pp. 156-62Hartl et al.. Morphologic parameters of normal swallowing events using single-shot fast spin echo dynamic MRI. Dysphagia (2003) vol.

18 (4) pp. 255-62Kuehn. A cineradiographic investigation of velar movement variables in two normals. The Cleft palate journal (1976) vol. 13 pp. 88-103Schipper et al.. “Triggered magnetic resonance tomography”. A new procedure for imaging soft tissue movement in dysphagia (initial re-

sults). HNO (1994) vol. 42 (3) pp. 177-81

Figure 4. (Left) T2-weighted anatomical reference scan showing dynamic scan field of view outlined in red, regional saturation areas outlined in yellow. (Center) Un-cropped dynamic image showing aliasing outside of reduced field of view. (Right) Dynamic image cropped to the reduced field of view and labeled with anatomic regions of interest.

Figure 1. Table showing effect of varying number of interleaves on sequence performance metrics. Plot displays the table columns for frame rate and BWPP. Values for the table and plot are based on simulations in the manufacturer-supplied development environment. BWPP (BandWidth Per Pixel) is defined as the inverse of readout duration (per shot). Temporal blur is defined as the time between the start of the first readout and the end of the last readout (per image). Frame duration is defined as the time between consecutive images. Overhead is the percentage of image capture time spent doing non-readout tasks (saturation, excitation, spoiling, etc.).

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Figure 2. Illustration showing additional images produced by moving window reconstruction with 3-interleaf step size compared to regular multi-shot spiral reconstruction.

Figure 3. Comparison of image acquisitions relative to self-paced swallows (red: oral stage, green: pharyngeal stage). Gated: Triggered by the onset of swallowing, parts of 4 images are collected during three repeated swallows. Retrospective: Untriggered acquisition captures images of swallowing phases out of order that must be retrospectively re ordered. Sequential, Prospective: Images are captured in playback order from a single swallowing event.

Bradley P. Sutton1,2, C. Conway1, Y. Bae2, A. Perlman2, D. Kuehn2

1Bioengineering Department, 2Department of Speech and Hearing ScienceUniversity of Illinois at Urbana-Champaign, Urbana-Champaign, IL, USA

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