Application of diffusion tensor imaging after glossectomy (2010)

Difficulty in visualizing the intricate architecture of the tongue has limited our understanding of its function during speech, mastication, and swallowing, as well as its adaptation to surgical procedures. Tractography visualization using diffusion tensor imaging (DTI), a semiautomatic technique, can detect and display the spatial distribution of the muscle fiber bundle orientations as three-dimensional (3D) trajectories in human and calf tongues.1,2 DTI is a magnetic resonance imaging (MRI) technique that measures the diffusivity of water in different directions3 and estimates fiber bundle orientation at each voxel, mathematically measuring the spatial distribution of diffusion tensors.4 It has been successfully applied to the study of neurologic conditions, including stroke, multiple sclerosis, brain tumors, and dementia. We have combined DTI with structural MRI as a means of observing residual tongue anatomy and yielding insight into the tongue's reconstruction after tumor resection in a glossectomy patient. A 34-year-old woman underwent a right partial glossectomy, primary closure, and a selective neck dissection for a stage 1 (T1N0M0) squamous cell carcinoma three and a half years prior to the present study. Clinically, the tumor, a 15 × 10-mm ulcer, was located in the mid third of the right lateral oral tongue. A 30 × 26 × 12-mm block was excised surgically and the pathologic study confirmed an 11 × 11-mm tumor. After surgery, the patient reported numbness of the right tongue, but no swallowing or speech problems. A 24-year-old man served as a control. This study was approved by the University of Maryland Institutional Review Board (protocol H28269). A 3-Tesla magnetic resonance system (Magnetom Trio, Siemens Medical Solutions, Erlangen, Germany) was used with a head and neck coil. The DTI parameters were: spin echo, echo planar imaging (EPI), field of view (FOV) = 240 mm, repetition time (TR) = 5000 ms, echo time (TE) = 68 ms, voxel size = 3.1 × 3.1 × 3.0 mm, matrix size = 64 × 64, slice thickness = 3 mm. Diffusion weighting was applied in 12 colinear directions, with a b value of 500 s/mm2 and three averages. Structural MRI T2-weighted images (T2) were taken as anatomic references in three orthogonal orientations. The parameters were: FOV = 240 mm, TR = 3310 ms, TE = 62 ms, voxel size = 0.9375 × 0.9375 × 3.0 mm, matrix size = 256 × 256. T2 has a much better spatial resolution than DTI and was therefore used to manually delineate a region of interest (ROI) on the target muscles bilaterally where they were clearly seen. Since the T2 and DTI images are spatially aligned, the ROI could be automatically transferred to the DTI and the corresponding fibers automatically determined, visualized, and quantified. Two muscles were targeted, due to tumor location and the surgical excision size: one extrinsic, the genioglossus (GG), and one intrinsic, the inferior longitudinalis (IL). The DTI data analysis and tractography were performed using dTV-II, implemented in VOLUME-ONE software (http://utradiology.umin.jp). The principal eigenvector from the three directions was assumed to correspond to the predominant fiber direction in the voxel. The fibers were estimated by connecting voxels according to the predominant fiber directions. Fibers were continuously tracked through voxels whenever the fractional anisotropy (FA) was > 0.18. Fractional anisotropy, which varies from 0 < FA < 1, uses the anisotropic relationship of the eigenvalues to determine the fiber direction. T2 MRI images for both the control subject and patient showed two target muscles, GG and IL, and the residual scar from the patient's surgery, as expected. In the control subject, the tongue septum was at midline and divided the GG symmetrically into right and left halves. The IL muscles were lateral to each GG muscle. In the patient, on the other hand, the septum and both GGs were deviated to the right and had lost the fan-shaped characteristics seen in normal tongues. Instead, there was a dark asymmetrical pattern in the tongue body that coincided with the area of excised tissue and surgical primary closure. Inferior longitudinalis (IL) fiber bundles resulting from the diffusion tensor imaging tractography in the control. Majority of both IL bundles are directed horizontally in the anterior-posterior direction. The three-dimensional straight lines in the colored globe indicate the main directions of the fiber bundles represented in the data. R, right; L, left; A, anterior; P, posterior; S, superior; I, inferior. The DTI tractography showed major changes in the IL, but little change in GG. Most of the IL bundles in the control were horizontal and oriented anterior-posterior (green), were symmetrical, and presented similar thickness (Fig 1). The patient's IL showed more striking changes. The right IL was thinner and shorter. Its interruption coincided with scar tissue in the T2 image. Although most of the left IL bundles were anteriorposterior (green), there were several bundles with right-left orientation (pink-red). The thickest red bundle (white arrow, Fig 2) depicted a direction change of some anterior-posterior left IL bundles to the right side of the tongue. The primary closure or tissue retraction after scar formation on the right side of the tongue may have caused this to occur. As expected, the GG showed a fan-shaped pattern in the control, but not in the patient. In the control, the anterior GG bundles were vertical (blue), the posterior were horizontal (green), and the medial GG bundles were colored with tones between blue and green. In the patient, the GG muscle bundles were mainly horizontal (green) and lateralized to the right side of the tongue, as observed in the T2 images. This is the first study to apply DTI to the tongue of a glossectomy patient in order to evaluate the 3D postsurgical myoarchitecture in vivo. Altered fiber directions and loss of continuity, length, and volume of each muscle bundle were seen in the glossectomy patient when compared to the normal subject. Residual tongue anatomy visualization may explain compensatory motor strategies postsurgery.5 Future use of DTI may facilitate diagnosis in presurgical patients with tongue cancer and contribute to our understanding of how the loss of tongue tissue and diverse reconstructive techniques might affect functional outcomes such as speech and swallowing. The authors would like to thank the staff of the Departments of Neural and Pain Sciences and Oral and Maxillofacial Surgery, University of Maryland Baltimore, for their continued support. Inferior longitudinalis (IL) fiber bundles resulting from the diffusion tensor imaging tractography in the patient. The right IL is thinner and shorter. Some contralateral IL bundles are directed horizontally in the right-left direction, seen as red bundles (white arrow). The three-dimensional straight lines in the colored globe indicate the main directions of the fiber bundles represented in the data. R, right; L, left; A, anterior; P, posterior; S, superior; I, inferior.