Impact of Multi-modality Monitoring Using Direct Electrical Stimulation to Determine Corticospinal Tract Shift and Integrity in Tumors using the Intraoperative MRI

Daria Krivosheya; Ganesh Rao; Sudhakar Tummala; Vinodh Kumar; Dima Suki; Dheigo C.A. Bastos; Sujit S. Prabhu

doi:10.1055/s-0039-1698383

Journal of Neurological Surgery Part A: Central European Neurosurgery, Inhaltsverzeichnis

J Neurol Surg A Cent Eur Neurosurg 2021; 82(04): 375-380
DOI: 10.1055/s-0039-1698383

Surgical Technique

Impact of Multi-modality Monitoring Using Direct Electrical Stimulation to Determine Corticospinal Tract Shift and Integrity in Tumors using the Intraoperative MRI

Daria Krivosheya

¹Department of Neurosurgery, Cleveland Clinic, Cleveland, Ohio, United States

,

Ganesh Rao

²Department of Neurosurgery, University of Texas MD Anderson Cancer Center, Houston, Texas, United States

,

Sudhakar Tummala

³Department of Neuro-Oncology, University of Texas MD Anderson Cancer Center, Houston, Texas, United States

,

Vinodh Kumar

⁴Department of Diagnostic Radiology, University of Texas MD Anderson Cancer Center, Houston, Texas, United States

,

Dima Suki

²Department of Neurosurgery, University of Texas MD Anderson Cancer Center, Houston, Texas, United States

,

Dheigo C.A. Bastos

²Department of Neurosurgery, University of Texas MD Anderson Cancer Center, Houston, Texas, United States

,

Sujit S. Prabhu

²Department of Neurosurgery, University of Texas MD Anderson Cancer Center, Houston, Texas, United States

› Institutsangaben

Abstract

Introduction Preserving the integrity of the corticospinal tract (CST) while maximizing the extent of tumor resection is one of the key principles of brain tumor surgery to prevent new neurologic deficits. Our goal was to determine the impact of the use of perioperative diffusion tensor imaging (DTI) fiber-tracking protocols for location of the CSTs, in conjunction with intraoperative direct electrical stimulation (DES) on patient neurologic outcomes. The role of combining DES and CST shift in intraoperative magnetic resonance imaging (iMRI) to enhance extent of resection (EOR) has not been studied previously.

Methods A total of 53 patients underwent resection of tumors adjacent to the motor gyrus and the underlying CST between June 5, 2009, and April 16, 2013. All cases were performed in the iMRI (BrainSuite 1.5 T). Preoperative DTI mapping and intraoperative cortical and subcortical DES including postoperative DTI mapping were performed in all patients. There were 32 men and 21 women with 40 high-grade gliomas (76%), 4 low-grade gliomas (8%), and 9 (17%) metastases. Thirty-four patients (64%) were newly diagnosed, and 19 (36%) had a previous resection. There were 31 (59%) right-sided and 22 (42%) left-sided tumors. Eighteen patients (34%) had a re-resection after the first intraoperative scan. Most patients had motor-only mapping, and one patient had both speech and motor mapping. Relative to the resection margin, the CST after the first iMRI was designated as having an outward shift (OS), inward shift (IS), or no shift (NS).

Results A gross total resection (GTR) was achieved in 41 patients (77%), subtotal resection in 4 (7.5%), and a partial resection in 8 (15%). Eighteen patients had a re-resection, and the mean EOR increased from 84% to 95% (p = 0.002). Of the 18 patients, 7 had an IS, 8 an OS, and in 3 NS was noted. More patients in the OS group had a GTR compared with the IS or NS groups (p = 0.004). Patients were divided into four groups based on the proximity of the tumor to the CST as measured from the preoperative scan. Group 1 (32%) included patients whose tumors were 0 to 5 mm from the CST based on preoperative scans; group 2 (28%), 6 to 10 mm; group 3 (13%), 11 to 15 mm; and group 4 (26%), 16 to 20 mm, respectively. Patients in group 4 had fewer neurologic complications compared with other groups at 1 and 3 months postoperatively (p = 0.001 and p = 0.007, respectively) despite achieving a similar degree of resection (p = 0.61). Furthermore, the current of intraoperative DES was correlated to the distance of the tumor to the CST, and the regression equation showed a close linear relationship between the two parameters.

Conclusions Combining information about intraoperative CST and DES in the iMRI can enhance resection in brain tumors (77% had a GTR). The relative relationship between the positions of the CST to the resection cavity can be a dynamic process that could further influence the surgeon's decision about the stimulation parameters and EOR. Also, the patients with an OS of the CST relative to the resection cavity had a GTR comparable with the other groups.

Keywords

corticospinal tract - intraoperative MRI - subcortical stimulation

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References
1 Duffau H, Capelle L, Denvil D. et al. Usefulness of intraoperative electrical subcortical mapping during surgery for low-grade gliomas located within eloquent brain regions: functional results in a consecutive series of 103 patients. J Neurosurg 2003; 98 (04) 764-778
2 Keles GE, Lundin DA, Lamborn KR, Chang EF, Ojemann G, Berger MS. Intraoperative subcortical stimulation mapping for hemispherical perirolandic gliomas located within or adjacent to the descending motor pathways: evaluation of morbidity and assessment of functional outcome in 294 patients. J Neurosurg 2004; 100 (03) 369-375
3 Kim SS, McCutcheon IE, Suki D. et al. Awake craniotomy for brain tumors near eloquent cortex: correlation of intraoperative cortical mapping with neurological outcomes in 309 consecutive patients. Neurosurgery 2009; 64 (05) 836-845 ; discussion 345–346
4 Krivosheya D, Prabhu SS, Weinberg JS, Sawaya R. Technical principles in glioma surgery and preoperative considerations. J Neurooncol 2016; 130 (02) 243-252
5 Krivosheya D, Prabhu SS. Combining functional studies with intraoperative MRI in glioma surgery. Neurosurg Clin N Am 2017; 28 (04) 487-497
6 Gasser T, Ganslandt O, Sandalcioglu E, Stolke D, Fahlbusch R, Nimsky C. Intraoperative functional MRI: implementation and preliminary experience. Neuroimage 2005; 26 (03) 685-693
7 Nimsky C, Ganslandt O, Merhof D, Sorensen AG, Fahlbusch R. Intraoperative visualization of the pyramidal tract by diffusion-tensor-imaging-based fiber tracking. Neuroimage 2006; 30 (04) 1219-1229
8 Hall WA, Liu H, Martin AJ, Truwit CL. Intraoperative magnetic resonance imaging. Top Magn Reson Imaging 2000; 11 (03) 203-212
9 Hall WA, Truwit CL. Intraoperative MR-guided neurosurgery. J Magn Reson Imaging 2008; 27 (02) 368-375
10 Hatiboglu MA, Weinberg JS, Suki D. et al. Impact of intraoperative high-field magnetic resonance imaging guidance on glioma surgery: a prospective volumetric analysis. Neurosurgery 2009; 64 (06) 1073-1081 ; discussion 1081
11 Nimsky C, Ganslandt O, Hastreiter P. et al. Intraoperative diffusion-tensor MR imaging: shifting of white matter tracts during neurosurgical procedures—initial experience. Radiology 2005; 234 (01) 218-225
12 Weingarten DM, Asthagiri AR, Butman JA. et al. Cortical mapping and frameless stereotactic navigation in the high-field intraoperative magnetic resonance imaging suite. J Neurosurg 2009; 111 (06) 1185-1190
13 Berman JI, Berger MS, Chung SW, Nagarajan SS, Henry RG. Accuracy of diffusion tensor magnetic resonance imaging tractography assessed using intraoperative subcortical stimulation mapping and magnetic source imaging. J Neurosurg 2007; 107 (03) 488-494
14 Kamada K, Todo T, Ota T. et al. The motor-evoked potential threshold evaluated by tractography and electrical stimulation. J Neurosurg 2009; 111 (04) 785-795
15 Mikuni N, Okada T, Nishida N. et al. Comparison between motor evoked potential recording and fiber tracking for estimating pyramidal tracts near brain tumors. J Neurosurg 2007; 106 (01) 128-133
16 Ozawa N, Muragaki Y, Nakamura R, Iseki H. Identification of the pyramidal tract by neuronavigation based on intraoperative diffusion-weighted imaging combined with subcortical stimulation. Stereotact Funct Neurosurg 2009; 87 (01) 18-24
17 De Witt Hamer PC, Robles SG, Zwinderman AH, Duffau H, Berger MS. Impact of intraoperative stimulation brain mapping on glioma surgery outcome: a meta-analysis. J Clin Oncol 2012; 30 (20) 2559-2565
18 Ojemann G, Ojemann J, Lettich E, Berger M. Cortical language localization in left, dominant hemisphere. An electrical stimulation mapping investigation in 117 patients. J Neurosurg 1989; 71 (03) 316-326
19 Taniguchi M, Cedzich C, Schramm J. Modification of cortical stimulation for motor evoked potentials under general anesthesia: technical description. Neurosurgery 1993; 32 (02) 219-226
20 Gasco J, Tummala S, Mahajan NM, Weinberg JS, Prabhu SS. Simultaneous use of functional tractography, neuronavigation-integrated subcortical white matter stimulation and intraoperative magnetic resonance imaging in glioma surgery: technical note. Stereotact Funct Neurosurg 2009; 87 (06) 395-398
21 Prabhu SS, Gasco J, Tummala S, Weinberg JS, Rao G. Intraoperative magnetic resonance imaging-guided tractography with integrated monopolar subcortical functional mapping for resection of brain tumors. Clinical article. J Neurosurg 2011; 114 (03) 719-726
22 Shahar T, Rozovski U, Marko NF. et al. Preoperative imaging to predict intraoperative changes in tumor-to-corticospinal tract distance: an analysis of 45 cases using high-field intraoperative magnetic resonance imaging. Neurosurgery 2014; 75 (01) 23-30
23 Seidel K, Beck J, Stieglitz L, Schucht P, Raabe A. The warning-sign hierarchy between quantitative subcortical motor mapping and continuous motor evoked potential monitoring during resection of supratentorial brain tumors. J Neurosurg 2013; 118 (02) 287-296
24 Raabe A, Beck J, Schucht P, Seidel K. Continuous dynamic mapping of the corticospinal tract during surgery of motor eloquent brain tumors: evaluation of a new method. J Neurosurg 2014; 120 (05) 1015-1024