Case Report: The Coronal Magnetic Resonance Imaging of Three-Dimensional Fast-Field Echo With Water-Selective Excitation Can Identify the Wrapping of Spinal Nerve Fibers Into Subdural Tumors Prior to Operation

Purpose In the present study, the authors intend to identify the spatial relationship between subdural tumors and spinal nerve fibers of cauda equina prior to operation using the coronal MRI of three-dimensional fast-field echo with water-selective excitation (CMRI). Methods In total, 30 case series with surgically and pathologically verified subdural tumors were enrolled in the present study. The spatial relationship between subdural tumors and spinal nerve fibers of the cauda equina was assessed via conventional MRI and CMRI by three experts prior to operation. The spatial relationship between subdural tumors and spinal nerve fibers of the cauda equina was classified using CMRI. The accuracy of imaging observation was determined via intraoperative observation. Results Though conventional MRI and gadolinium (Gd)-enhanced MRI (Gd MRI) cannot identify the spatial relationship between subdural tumors and spinal nerve fibers of cauda equina in all cases, CMRI can identify it prior to operation and divide the spatial relationship of spinal nerve fibers of cauda equina with subdural tumors into three types. CMRI shows higher sensitivity (97.44%) and specificity (90.47%) in identifying the spatial relationship of spinal nerve fibers of cauda equina with subdural tumors. Additionally, CMRI also showed a substantial agreement with a kappa value of 0.78. Conclusion Herein, the authors first describe a potential novel application that CMRI can successfully identify the spatial relationship between subdural tumors and spinal nerve fibers of cauda equina prior to operation, which play an essential role in making a prudent surgical plan and preventing postoperative nerve damage. Summary Intraoperative observation confirms spinal nerve fibers of cauda equina are often wrapped into subdural tumors of the thoracolumbar and lumbar region, which can result in a high rate of sensory and motor dysfunction after the operation due to the unconscious about the wrapping of nerves into subdural tumors prior to operation. To date, there is not an effective strategy to identify the wrapping before operation.


Case Series
A total of thirty patients with subdural tumors who underwent surgical treatment in our department were enrolled in this study and included 16 men and 14 women with an average age of 53.4 ± 13.06 years old, ranging from 27 to 86 years old. The subdural tumors of 4 cases were located in the cervical segment, 6 cases in the thoracic segment, 7 cases in the thoracolumbar segment, and 13 cases in the lumbar segment.
Our pre-study found that it is very difficult in identifying the spatial relationship between subdural tumors and spinal nerve fibers in cervical and thoracic segments using CMRI. Therefore, only the subdural tumors located in thoracolumbar and lumbar segments were involved in subsequent research. Clinical data are shown in Table 1. This study was approved by the medical ethics committee of our hospital and all patients provided their signed informed consent.

Imaging
Scanning parameters of CMRI refer to our previous research (5). Magnetic resonance nerve root water imaging was performed on the spine of patients with the 3.0T Superconducting MRI scanning system (Skyra; Siemens Healthcare, Erlangen, Germany) with the following scanning parameters: TR 2000 ms, TE 32 ms, FOV 32 cm, turning angle 20 • , layer thickness 1 mm, continuous scanning without interval, matrix 352 × 256, with 2 acquisition times. The coronal images were reconstructed by maximum signal intensity projection (MIP) and stereoscopic fluoroscopy (VRT) on the ADW 4.6 software, followed by the 3D rotational observation.

Classification of the Spatial Relationship Between Tumor and Nerves
The spatial relationship between the tumor and the spinal nerve can be classified into three types. Type I: tumor compresses nerves, the nerves get displaced, but the nerves pass around the tumor and no nerve fibers enter or pass through the tumor. Type II: a part of the nerves enters the tumor and terminates at the end of the tumor. There is no nerve fiber perforation at the distal end of the tumor. Type III: some nerves enter and pass through the tumor.

Statistics
Statistical analysis was performed using the SPSS version 25 for Windows (SPSS Inc., Chicago, IL, USA). Inter-observer agreement was evaluated by kappa analysis as described elsewhere (6). A kappa value of 0-0.2 was considered a slight agreement, 0.21 to 0.4 as a fair agreement, 0.41 to 0.6 as a moderate agreement, 0.61 to 0.8 as a substantial agreement, 0.81 to <1 as an almost perfect agreement, and 1.00 as the perfect agreement. The chi-squared test was performed to analyze the accuracy of identifying the spatial relationship between the subdural tumor and the nerve on CMRI. An intraoperative observation was considered the gold standard. The sensitivity and specificity were calculated according to the gold standard. P < 0.05 was considered to indicate statistical significance.

RESULTS
Clinical data and follow-up information are shown in Table 1. CMRI can clearly demonstrate the spatial relationships between the nerve fibers of the spinal cord and subdural tumors. The sensitivity and specificity of CMRI in ascertaining the relationship between the tumor and the spinal nerve were 97.44 and 90.47%. Additionally, CMRI showed a kappa value of 0.78, which indicated that it was reliable. The spatial relationship between the nerve fibers of the spinal cord and subdural tumors was divided into three types, as shown in the typical case (Figures 1-3). Meanwhile, the limitation of CMRI was displayed in Supplementary Figure S1. The nerve fibers are perfectly displayed in Supplementary Figure S2.

DISCUSSION
Magnetic resonance nerve root water imaging is a T2 weighted imaging technology that suppresses the fat components between the peripheral and internal nervous tracts and obtains images of only the liquid in the inner membrane of the nervous tract based on heavy T2 weighting combined with fat suppression technology (7). Shen et al. (8) found that, unlike conventional MRI, magnetic resonance nerve root water imaging could clearly depict the full length of the spinal nerve root. Byun et al. (9) observed that the technology could additionally demonstrate the 3D relationship between the nerve root and the intervertebral disc, which is conducive to the discovery of extreme lateral disc herniation. Our previous study confirmed that the sensitivity and specificity of the technique in identifying extreme lateral disc herniation are better than those of conventional MRI (10).
Subsequently, it has also been verified by our other study that the CMRI is beneficial in the differential diagnosis of tumor-like disc herniation (5). Considering the advantages of this approach in spinal cord nervous tract imaging, the authors tried to analyze whether it could determine the relationship between subdural tumor and spinal cord nervous tract preoperatively to aid in surgical planning and prognosis prediction.
In the present study, we found that CMRI not only can clearly identify the spatial relationship between the subdural tumor of thoracolumbar and lumbar segments and the spinal cord nervous tract prior to the operation but also can determine that the nerve fibers wrapped into the tumor belong to which nerve root is, as typical case 4. It was extremely helpful for the surgeon to make clear whether the subdural tumor can be totally resected prior to operation via CMRI. Moreover, CMRI can assist the surgeon in making decisions on whether the nerve fibers wrapped into a tumor should be resected by weighing the pros and cons. Meanwhile, the surgeon can also inform the patients about the severity of neurological impairment after the operation. Subsequently, we assessed the sensitivity, specificity, and reliability of CMRI in identifying the spatial relationship between the nerve fibers of the spinal cord and subdural tumor. We found that CMRI presented a high sensitivity, specificity, and reliability. This indicated that CMRI holds significance in guiding spine surgeons and neurosurgeons before surgical treatment of subdural tumors.
There are still some limitations to our study. Unlike cauda equina nerve in thoracolumbar and lumbar segments, CMRI cannot identify the spatial relationship of the subdural tumor with nerve fibers of the spinal cord in cervical and thoracic segments. An alternative strategy for the identification is diffusion tensor imaging. However, the reliability of diffusion tensor imaging still needs to be improved due to magnetic susceptibility artifacts at the bone-tissue interface. Only meningioma, neurilemmoma, and teratoma were involved in the study due to the small sample size. A multicenter study ought to be considered using a larger sample size in order to support or refute our findings.

DATA AVAILABILITY STATEMENT
The raw data supporting the conclusions of this article will be made available by the authors, without undue reservation.

ETHICS STATEMENT
Written informed consent was obtained from the individual(s) for the publication of any potentially identifiable images or data included in this article.

AUTHOR CONTRIBUTIONS
TT and JJ contributed to the study concept and design. JYu, JYi, and JZ participated in the data acquisition and analysis. JJ, JYi, and XC evaluated the CMRI. TT, JJ, and XC performed the surgery and perioperative management on the patient. TT and XC wrote the manuscript with contributions from all coauthors. All authors contributed to the article and approved the submitted version.

ACKNOWLEDGMENTS
We thank our patients and their legal representatives for consenting to the publication of this case series.

SUPPLEMENTARY MATERIAL
The Supplementary Material for this article can be found online at: https://www.frontiersin.org/articles/10.3389/fneur. 2022.945299/full#supplementary-material Supplementary Table S1 | The type of the spatial relationship between the nerve fibers and the thoracolumbar junction or lumbar subdural tumor was identified via preoperative CMRI and intraoperative observation.