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Jeffrey I. Berman, Mitchel S. Berger, Pratik Mukherjee, and Roland G. Henry

Object. The goal of this study was to use diffusion-tensor (DT) magnetic resonance (MR) imaging to track fibers combined with cortical stimulation mapping to delineate descending motor pathways. Subcortical localization of motor pathways in relation to a glioma may provide critical information to guide tumor resection and prevent surgical morbidity.

Methods. Eleven adult patients harboring gliomas underwent MR imaging 1 day prior to image-guided intraoperative cortical motor mapping and tumor resection. Screens depicting 27 cortical motor sites on a surgical navigation system were saved to launch DT imaging of fiber tracks of descending motor pathways. The position and organization of motor tracts were visualized by fiber tracking. Tracks from 16 motor stimulation sites followed descending pathways from the precentral gyrus, through the corona radiata and internal capsule, and into the cerebral peduncle. These tracks were also observed on DT images to diverge along crossing white matter bundles (four patients) and to terminate or deviate in regions of peritumoral vasogenic edema (five patients).

Conclusions. The use of precise intraoperative cortical mapping information and DT images of fiber tracks can reveal the course of motor pathways beneath the cortex. The subcortical fiber tracks generated are consistent with the known anatomical course and somatotopic organization of the motor tract in relation to its cortical origins. Tracking fibers by using DT imaging in combination with functional localization has the potential to reduce surgical morbidity by revealing subcortical connections of the functional cortex.

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Jeffrey I. Berman, Mitchel S. Berger, Sungwon Chung, Srikantan S. Nagarajan, and Roland G. Henry

Object

Resecting brain tumors involves the risk of damaging the descending motor pathway. Diffusion tensor (DT)–imaged fiber tracking is a noninvasive magnetic resonance (MR) technique that can delineate the subcortical course of the motor pathway. The goal of this study was to use intraoperative subcortical stimulation mapping of the motor tract and magnetic source imaging to validate the utility of DT-imaged fiber tracking as a tool for presurgical planning.

Methods

Diffusion tensor-imaged fiber tracks of the motor tract were generated preoperatively in nine patients with gliomas. A mask of the resultant fiber tracks was overlaid on high-resolution T1- and T2-weighted anatomical MR images and used for stereotactic surgical navigation. Magnetic source imaging was performed in seven of the patients to identify functional somatosensory cortices. During resection, subcortical stimulation mapping of the motor pathway was performed within the white matter using a bipolar electrode.

Results

A total of 16 subcortical motor stimulations were stereotactically identified in nine patients. The mean distance between the stimulation sites and the DT-imaged fiber tracks was 8.7 ±3.1 mm (±standard deviation). The measured distance between subcortical stimulation sites and DT-imaged fiber tracks combines tracking technique errors and all errors encountered with stereotactic navigation.

Conclusions

Fiber tracks delineated using DT imaging can be used to identify the motor tract in deep white matter and define a safety margin around the tract.

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Seunggu J. Han, Ramin A. Morshed, Irene Troncon, Kesshi M. Jordan, Roland G. Henry, Shawn L. Hervey-Jumper, and Mitchel S. Berger

OBJECTIVE

Herein, the authors report their experience with intraoperative stimulation mapping to locate the descending subcortical motor pathways in patients undergoing surgery for hemispheric gliomas within or adjacent to the rolandic cortex, with particular description of the morbidity and functional outcomes associated with this technique.

METHODS

This is a retrospective analysis of patients who, in the period between 1997 and 2016, had undergone resection of hemispheric perirolandic gliomas within or adjacent to descending motor pathways. Data regarding intraoperative stimulation mapping and patient postoperative neurological status were collected.

RESULTS

Of 702 patients, stimulation mapping identified the descending motor pathways in 300 cases (43%). A new or worsened motor deficit was seen postoperatively in 210 cases (30%). Among these 210 cases, there was improvement in motor function to baseline levels by 3 months postoperatively in 161 cases (77%), whereas the deficit remained in 49 cases (23%). The majority (65%) of long-term deficits (persisting beyond 3 months) were mild or moderate (antigravity strength or better). On multivariate analysis, patients in whom the subcortical motor pathways had been identified with stimulation mapping during surgery were more likely to develop an additional and/or worsened motor deficit postoperatively than were those in whom the subcortical pathways had not been found (45% vs 19%, respectively, p < 0.001). This difference remained when considering the likelihood of a long-term deficit (i.e., persisting > 3 months; 12% vs 3.2%, p < 0.001). A higher tumor grade and the presence of a preoperative motor deficit were also associated with higher rates of motor deficits persisting long-term. A region of restricted diffusion adjacent to the resection cavity was seen in 20 patients with long-term deficits (41%) and was more common in cases in which the motor pathways were not identified (69%). Long-term deficits that occur in settings in which the subcortical motor pathways are not identified seem in large part due to ischemic injury to descending tracts.

CONCLUSIONS

Stimulation mapping allows surgeons to identify the descending motor pathways during resection of tumors in perirolandic regions and to attain an acceptable rate of morbidity in these high-risk cases.

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Maria Luisa Mandelli, Mitchel S. Berger, Monica Bucci, Jeffrey I. Berman, Bagrat Amirbekian, and Roland G. Henry

Object

The aim of this paper was to validate the diffusion tensor imaging (DTI) model for delineation of the corticospinal tract using cortical and subcortical white matter electrical stimulation for the location of functional motor pathways.

Methods

The authors compare probabilistic versus deterministic DTI fiber tracking by reconstructing the pyramidal fiber tracts on preoperatively acquired DTI in patients with brain tumors. They determined the accuracy and precision of these 2 methods using subcortical stimulation points and the sensitivity using cortical stimulation points. The authors further explored the reliability of these methods by estimation of the potential that the found connections were due to a random chance using a novel neighborhood permutation method.

Results

The probabilistic tracking method delineated tracts that were significantly closer to the stimulation points and was more sensitive than deterministic DTI fiber tracking to define the tracts directed to the motor sites. However, both techniques demonstrated poor sensitivity to finding lateral motor regions.

Conclusions

This study highlights the importance of the validation and quantification of preoperative fiber tracking with the aid of electrophysiological data during the surgery. The poor sensitivity of DTI to delineate lateral motor pathways reported herein suggests that DTI fiber tracking must be used with caution and only as adjunctive data to established methods for motor mapping.

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Derek G. Southwell, Marco Riva, Kesshi Jordan, Eduardo Caverzasi, Jing Li, David W. Perry, Roland G. Henry, and Mitchel S. Berger

OBJECTIVE

The dominant inferior parietal lobule (IPL) contains cortical and subcortical regions essential for language. Although resection of IPL tumors could result in language deficits, little is known about the likelihood of postoperative language morbidity or the risk factors predisposing to this outcome.

METHODS

The authors retrospectively examined a series of patients who underwent resections of gliomas from the dominant IPL. Postoperative language outcomes were characterized across the patient population. To identify factors associated with postoperative language morbidity, the authors then compared features between those patients who experienced postoperative deficits and those who experienced no postoperative language dysfunction.

RESULTS

Twenty-four patients were identified for analysis. Long-term language deficits occurred in 29.2% of patients (7 of 24): 3 of these patients had experienced preoperative language deficits, whereas new long-term language deficits occurred in 4 patients (16.7%; 4 of 24). Of those patients who exhibited preoperative language deficits, 62.5% (5 of 8) experienced long-term resolution of their language deficits with surgical treatment. All patients underwent intraoperative brain mapping by direct electrical stimulation. Awake, intraoperative cortical language mapping was performed on 17 patients (70.8%). Positive cortical language sites were identified in 23.5% of these patients (4 of 17). Awake, intraoperative subcortical language mapping was performed in 8 patients (33.3%). Positive subcortical language sites were identified in 62.5% of these patients (5 of 8). Patients with positive cortical language sites exhibited a higher rate of long-term language deficits (3 of 4, 75%), compared with those who did not (1 of 13, 7.7%; p = 0.02). Although patients with positive subcortical language sites exhibited a higher rate of long-term language deficits than those who exhibited only negative sites (40.0% vs 0.0%, respectively), this difference was not statistically significant (p = 0.46). Additionally, patients with long-term language deficits were older than those without deficits (p < 0.05).

CONCLUSIONS

In a small number of patients with preoperative language deficits, IPL glioma resection resulted in improved language function. However, in patients with intact preoperative language function, resection of IPL gliomas may result in new language deficits, especially if the tumors are diffuse, high-grade lesions. Thus, language-dominant IPL glioma resection is not risk-free, yet it is safe and its morbidity can be reduced by the use of cortical and subcortical stimulation mapping.

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Eduardo Caverzasi, Shawn L. Hervey-Jumper, Kesshi M. Jordan, Iryna V. Lobach, Jing Li, Valentina Panara, Caroline A. Racine, Vanitha Sankaranarayanan, Bagrat Amirbekian, Nico Papinutto, Mitchel S. Berger, and Roland G. Henry

OBJECT

Diffusion MRI has uniquely enabled in vivo delineation of white matter tracts, which has been applied to the segmentation of eloquent pathways for intraoperative mapping. The last decade has also seen the development from earlier diffusion tensor models to higher-order models, which take advantage of high angular resolution diffusion-weighted imaging (HARDI) techniques. However, these advanced methods have not been widely implemented for routine preoperative and intraoperative mapping.

The authors report on the application of residual bootstrap q-ball fiber tracking for routine mapping of potentially functional language pathways, the development of a system for rating tract injury to evaluate the impact on clinically assessed language function, and initial results predicting long-term language deficits following glioma resection.

METHODS

The authors have developed methods for the segmentation of 8 putative language pathways including dorsal phonological pathways and ventral semantic streams using residual bootstrap q-ball fiber tracking. Furthermore, they have implemented clinically feasible preoperative acquisition and processing of HARDI data to delineate these pathways for neurosurgical application. They have also developed a rating scale based on the altered fiber tract density to estimate the degree of pathway injury, applying these ratings to a subset of 35 patients with pre- and postoperative fiber tracking. The relationships between specific pathways and clinical language deficits were assessed to determine which pathways are predictive of long-term language deficits following surgery.

RESULTS

This tracking methodology has been routinely implemented for preoperative mapping in patients with brain gliomas who have undergone awake brain tumor resection at the University of California, San Francisco (more than 300 patients to date). In this particular study the authors investigated the white matter structure status and language correlation in a subcohort of 35 subjects both pre- and postsurgery. The rating scales developed for fiber pathway damage were found to be highly reproducible and provided significant correlations with language performance. Preservation of the left arcuate fasciculus (AF) and the temporoparietal component of the superior longitudinal fasciculus (SLF-tp) was consistent in all patients without language deficits (p < 0.001) at the long-term follow-up. Furthermore, in patients with short-term language deficits, the AF and/or SLF-tp were affected, and damage to these 2 pathways was predictive of a long-term language deficit (p = 0.005).

CONCLUSIONS

The authors demonstrated the successful application of q-ball tracking in presurgical planning for language pathways in brain tumor patients and in assessing white matter tract integrity postoperatively to predict long-term language dysfunction. These initial results predicting long-term language deficits following tumor resection indicate that postoperative injury to dorsal language pathways may be prognostic for long-term clinical language deficits.

Study results suggest the importance of dorsal stream tract preservation to reduce language deficits in patients undergoing glioma resection, as well as the potential prognostic value of assessing postoperative injury to dorsal language pathways to predict long-term clinical language deficits.