3D Cranial Nerve Imaging, a Novel MR Neurography Technique Using Black-Blood STIR TSE with a Pseudo Steady-State Sweep and Motion-Sensitized Driven Equilibrium Pulse for the Visualization of the Extraforaminal Cranial Nerve Branches

SUMMARY: This study investigated the feasibility of a 3D black-blood STIR TSE sequence with a pseudo steady-state sweep and motion-sensitized driven equilibrium pulse for extraforaminal cranial nerve imaging on a 3T system. Assessments of healthy volunteers showed near-perfect agreement in nerve visualization with excellent to good visualization of the extraforaminal trigeminal, greater occipital, and facial nerves. Suppression of surrounding tissues was excellent to good. 3D cranial nerve imaging can produce nerve selective imaging of extraforaminal cranial and spinal nerve branches.

B eing the largest cranial nerve, the trigeminal nerve-more specifically, its inferior alveolar and lingual branches-is frequently damaged during dental, oral, and maxillofacial surgical procedures. 1 Moreover, it can be subject to myriad disease entities such as inflammatory, infectious, neoplastic, and congenital pathology. MR imaging has been widely applied to the visualization of cranial nerves. 2 Intracranial trajectories such as nuclear and supranuclear, as well as cisternal segments, can be well depicted on routine MR imaging sequences. The cisternal segment is typically visualized using constructive interference in steady state and 3D heavily T2WI. 3 However, visualization of the extracranial peripheral branches on 3D T2WI remains a challenge because of their small diameters, tortuous courses, movement and susceptibility artifacts, and the presence of blood vessels in close proximity, which can all confound nerve visualization. 4 B1 and B0 inhomogeneities further lead to poor fat suppression and low SNR, and the use of multiple echoes to improve water and fat separation increases acquisition times considerably, making patient compliance difficult. To address these problems, we developed a novel black-blood 3D STIR TSE sequence for extraforaminal cranial nerve imaging (3D CRANI) on a 3T system and here describe its assessment.

Description of Technique
The 3D CRANI is a 3D TSE STIR black-blood sequence that uses a pseudo steady-state (PSS) sweep in combination with a motionsensitized driven equilibrium (MSDE) pulse. We used STIR in combination with MSDE to ensure that signals from fat, muscle, and blood are suppressed uniformly across the field of view. The PSS sweep is designed such that the signal is smoothly varying during a long TSE shot to keep the signal strength approximately constant. This means that the flip angle sweep is not calculated based on specific tissue parameters (T1, T2). In this manner, it helps us to reduce the T2 decay for a range of tissues, which makes the sequence less sensitive to tissue dependencies. For the PSS functionality, minimum, middle, and maximum angles need to be defined, and 4 intermediate flip angles are used to asymptotically approach the minimum flip angle defined within the sequence (Online Supplemental Data). After reaching the minimum angle, nonlinear interpolation is used to calculate an optimum sweep according to the PSS principle while trying to keep the signal constant. 5 The middle angle is defined at the specified effective TE. After definition of the middle angle, the refocusing angles are increased linearly to the maximum defined angle.
Finally, compressed sensing is added to reduce the acquisition time. The sequence was optimized by comparing it with existing nerve-selective sequences until satisfactory and robust results were obtained, with particular attention being paid to artifact reduction (Online Supplemental Data).

Imaging Analysis
Three orthogonal planes, as well as a plane following the course of the nerve trajectory using MPR and MIP, were reconstructed using the Volume postprocessing package (Philips Healthcare). MIP images with a thickness of 5 mm and gap of À0.5 mm (4.5mm overlap) allowed for the best demonstration of the selected nerve trajectory. The images were analyzed by 2 fixed and independent observers with expertise in cranial nerve imaging. First, a training session was held to familiarize the observers with the grading scales. Then, for the subsequent evaluations, the observers were blinded to each other's scoring. Arterial, venous, and fat suppression were graded on a 3-point Likert scale (0 ¼ unsuppressed and nondiagnostic; 1 ¼ moderately suppressed but diagnostic; 2 ¼ excellent suppression). A nerve scoring system using a 5-point Likert scale (4 ¼ excellent; 3 ¼ good; 2 ¼ fair;1 ¼ poor; 0 ¼ none) was adopted from Fujii et al 6 to evaluate the signal continuity of the following nerves over a predetermined trajectory. The evaluated trajectory of the inferior alveolar (V3) and lingual (V3) nerves starts at the oval foramen and stops at the mental foramen and the submandibular duct, respectively. The facial nerve (VII) trajectory starts in the labyrinthine portion in the temporal bone and stops at the anterior edge of the parotid. The greater occipital nerve (C2-C3) trajectory starts posterior to the axis and stops before piercing the trapezius muscle. 6

Statistical Analysis
All statistical analyses were performed using SPSS version 26.0 (IBM). Interobserver agreement on the Likert scales was tested using weighted kappa statistics with quadratic weights. A P value less than .05 was considered statistically significant.

RESULTS
There was a statistically significant nearperfect agreement between the 2 observers, except in the visualization of the extracranial portion of the facial nerve, for which the agreement was still considered to be very good (independent observer scores are illustrated in the Online Supplemental Data). The strength of agreement ranged from very good to excellent for all parameters (Table). Venous suppression was evaluated as excellent except in 2 cases in which it was considered "moderately suppressed." These 2 cases also had the lowest scores for the other variables observed. When the independent nerve scoring results were evaluated, the facial nerve had the lowest scores. The visualizations of the trigeminal and greater occipital nerve branches were rated as good to excellent. The

DISCUSSION
This technical note successfully demonstrates the use of 3D CRANI, a modified black-blood STIR TSE sequence for nerveselective imaging of peripheral cranial and spinal nerve branches. Diffusion-weighted prepulsing by MSDE for MR neurography purposes was first described by Yoneyama et al 7 and further demonstrated for brachial plexus imaging by Klupp et al. 8 This study is innovative in the sense that an MSDE pulse was applied in combination with a PSS sweep to further optimize nerve-enhanced imaging within clinically feasible acquisition times. The results from our study indicate excellent interobserver agreement. Moreover, the scoring of the images indicates moderate to excellent suppression of surrounding tissues. Chhabra et al 9,10 published several papers on cranial nerve imaging and advocate several sequences for clinical evaluations, including a STIR TSE sequence when magnetic field inhomogeneities are expected. 11,12 However, their main imaging method for MR neurography involves diffusion-weighted reversed fast imaging with steady-state free precession, which is applied using gradient-echo imaging. In the past, gradient-echo imaging was preferred because of its short acquisition times. However, with new techniques such as those illustrated in this study, STIR sequences with reasonable acquisition times, low artifact susceptibility, and excellent fat suppression have become possible. The current limitations appear to be similar signal intensities for nerve and (intraparotid) lymphoid tissue, unpredictable visualization of nerves with a diameter less than 0.9 mm, and imperfect venous suppression of the pterygoid plexus. A future large prospective study will be designed to validate this sequence in both healthy and patient populations, comparing 3D CRANI with existing protocols.

CONCLUSIONS
3D CRANI can produce nerve-selective imaging of the trigeminal, facial, and greater occipital extraforaminal nerve branches, with excellent interobserver agreement and within clinically feasible acquisition times. Prospective studies are needed to further evaluate and validate its clinical use.