Tractography guides the approach for resection of thalamopeduncular tumors

Acta Neurochir (2017) 159:1597–1601

Thalamopeduncular tumors arise at the junction of the inferior thalamus and cerebral peduncle, and present with a common clinical syndrome of progressive spastic hemiparesis.

Method Formal preoperative magnetic resonance imaging (MRI) and diffusion tensor imaging (DTI) were performed. Postoperative MRI was obtained to evaluate the extent of tumor resection. A prospective analysis of clinical outcomes was then conducted by the senior author.

Conclusions Preoperative tractography is a useful adjunct to surgical planning in tumors that displace motor pathways. Gross total resection of pilocytic astrocytomas usually results in cure, and therefore should be entertained when developing treatment strategies for thalamopeduncular tumors of childhood.

A method for safely resecting anterior butterfly gliomas

J Neurosurg 126:1795–1811, 2017

Gliomas invading the anterior corpus callosum are commonly deemed unresectable due to an unacceptable risk/benefit ratio, including the risk of abulia. In this study, the authors investigated the anatomy of the cingulum and its connectivity within the default mode network (DMN). A technique is described involving awake subcortical mapping with higher attention tasks to preserve the cingulum and reduce the incidence of postoperative abulia for patients with so-called butterfly gliomas.

METHODS The authors reviewed clinical data on all patients undergoing glioma surgery performed by the senior author during a 4-year period at the University of Oklahoma Health Sciences Center. Forty patients were identified who underwent surgery for butterfly gliomas. Each patient was designated as having undergone surgery either with or without the use of awake subcortical mapping and preservation of the cingulum. Data recorded on these patients included the incidence of abulia/akinetic mutism. In the context of the study findings, the authors conducted a detailed anatomical study of the cingulum and its role within the DMN using postmortem fiber tract dissections of 10 cerebral hemispheres and in vivo diffusion tractography of 10 healthy subjects.

RESULTS Forty patients with butterfly gliomas were treated, 25 (62%) with standard surgical methods and 15 (38%) with awake subcortical mapping and preservation of the cingulum. One patient (1/15, 7%) experienced postoperative abulia following surgery with the cingulum-sparing technique. Greater than 90% resection was achieved in 13/15 (87%) of these patients.

CONCLUSIONS This study presents evidence that anterior butterfly gliomas can be safely removed using a novel, attention-task based, awake brain surgery technique that focuses on preserving the anatomical connectivity of the cingulum and relevant aspects of the cingulate gyrus.

 

Probabilistic versus deterministic tractography for delineation of the cortico-subthalamic hyperdirect pathway in patients with Parkinson disease selected for deep brain stimulation

J Neurosurg 126:1657–1668, 2017

Diffusion-weighted MRI (DWI) and tractography allows noninvasive mapping of the structural connections of the brain, and may provide important information for neurosurgical planning. The hyperdirect pathway, connecting the subthalamic nucleus (STN) with the motor cortex, is assumed to play a key role in mediating the effects of deep brain stimulation (DBS), which is an effective but poorly understood treatment for Parkinson disease. This study aimed to apply recent methodological advances in DWI acquisition and analysis to the delineation of the hyperdirect pathway in patients with Parkinson disease selected for surgery.

METHODS High spatial and angular resolution DWI data were acquired preoperatively from 5 patients with Parkinson disease undergoing DBS. The authors compared the delineated hyperdirect pathways and associated STN target maps generated by 2 different tractography methods: a tensor-based deterministic method, typically available in clinical settings, and an advanced probabilistic method based on constrained spherical deconvolution. In addition, 10 highresolution data sets with the same scanning parameters were acquired from a healthy control participant to assess the robustness of the tractography results.

RESULTS Both tractography approaches identified connections between the ipsilateral motor cortex and the STN. However, the 2 methods provided substantially different target regions in the STN, with the target center of gravity differing by > 1.4 mm on average. The probabilistic method (based on constrained spherical deconvolution) plausibly reconstructed a continuous set of connections from the motor cortex, terminating in the dorsolateral region of the STN. In contrast, the tensor-based method reconstructed a comparatively sparser and more variable subset of connections. Furthermore, across the control scans, the probabilistic method identified considerably more consistent targeting regions within the STN compared with the deterministic tensor-based method, which demonstrated a 1.9–2.4 times higher variation.

CONCLUSIONS These data provide a strong impetus for the use of a robust probabilistic tractography framework based on constrained spherical deconvolution, or similar advanced DWI models, in clinical settings. The inherent limitations and demonstrated inaccuracy of the tensor-based method leave it questionable for use in high-precision stereotactic DBS surgery. The authors have also described a straightforward method for importing tractography-derived information into any clinical neuronavigation system, based on the generation of track-density images.

Human Connectome-Based Tractographic Atlas of the Brainstem Connections and Surgical Approaches

Human Connectome-Based Tractographic Atlas of the Brainstem Connections and Surgical Approaches

Neurosurgery 79:437–455, 2016

The brainstem is one of the most challenging areas for the neurosurgeon because of the limited space between gray matter nuclei and white matter pathways. Diffusion tensor imaging–based tractography has been used to study the brainstem structure, but the angular and spatial resolution could be improved further with advanced diffusion magnetic resonance imaging (MRI).

OBJECTIVE: To construct a high–angular/spatial resolution, wide-population–based, comprehensive tractography atlas that presents an anatomical review of the surgical approaches to the brainstem.

METHODS: We applied advanced diffusion MRI fiber tractography to a population-based atlas constructed with data from a total of 488 subjects from the Human Connectome Project-488. Five formalin-fixed brains were studied for surgical landmarks. Luxol Fast Blue–stained histological sections were used to validate the results of tractography.

RESULTS: We acquired the tractography of the major brainstem pathways and validated them with histological analysis. The pathways included the cerebellar peduncles, corticospinal tract, corticopontine tracts, medial lemniscus, lateral lemniscus, spinothalamic tract, rubrospinal tract, central tegmental tract, medial longitudinal fasciculus, and dorsal longitudinal fasciculus. Then, the reconstructed 3-dimensional brainstem structure was sectioned at the level of classic surgical approaches, namely supracollicular, infracollicular, lateral mesencephalic, perioculomotor, peritrigeminal, anterolateral (to the medulla), and retro-olivary approaches.

CONCLUSION: The advanced diffusion MRI fiber tracking is a powerful tool to explore the brainstem neuroanatomy and to achieve a better understanding of surgical approaches.

Identifying preoperative language tracts and predicting postoperative functional recovery using HARDI q-ball fiber tractography in patients with gliomas

Identifying preoperative language tracts and predicting postoperative functional recovery using HARDI q-ball ber tractography in patients with gliomas

J Neurosurg 125:33–45, 2016

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.

Does Navigated Transcranial Stimulation Increase the Accuracy of Tractography?

Does Navigated Transcranial Stimulation Increase the Accuracy of Tractography?

Neurosurgery 0:1–10, 2015

Tractography based on diffusion tensor imaging has become a popular tool for delineating white matter tracts for neurosurgical procedures.

OBJECTIVE: To explore whether navigated transcranial magnetic stimulation (nTMS) might increase the accuracy of fiber tracking.

METHODS: Tractography was performed according to both anatomic delineation of the motor cortex (n = 14) and nTMS results (n = 9). After implantation of the definitive electrode, stimulation via the electrode was performed, defining a stimulation threshold for eliciting motor evoked potentials recorded during deep brain stimulation surgery. Others have shown that of arm and leg muscles. This threshold was correlated with the shortest distance between the active electrode contact and both fiber tracks. Results were evaluated by correlation to motor evoked potential monitoring during deep brain stimulation, a surgical procedure causing hardly any brain shift.

RESULTS: Distances to fiber tracks clearly correlated with motor evoked potential thresholds. Tracks based on nTMS had a higher predictive value than tracks based on anatomic motor cortex definition (P < .001 and P = .005, respectively). However, target site, hemisphere, and active electrode contact did not influence this correlation.

CONCLUSION: The implementation of tractography based on nTMS increases the accuracy of fiber tracking. Moreover, this combination of methods has the potential to become a supplemental tool for guiding electrode implantation.

Surgical results of tumor resection using tractography-integrated navigation-guided fence-post catheter techniques and motor-evoked potentials for preservation of motor function in patients with glioblastomas near the pyramidal tracts

Surgical results of tumor resection using tractography-integrated

Neurosurg Rev (2015) 38:293–307

The current optimal surgery for glioblastomas (GBMs) near the pyramidal tract (PT) is to remove as much tumor as possible and to preserve motor function. The purpose of this study is to investigate the usefulness of tractography integrated navigation-guided fence-post catheter techniques and motor-evoked potentials (MEPs) for preserving postoperative motor function after GBM surgery.

We retrospectively examined 49 patients who underwent resection for GBM near the PT. Diffusion tensor (DT) imaging-based tractography of the PT was performed preoperatively and integrated into the navigation system. When possible, silicon catheters were used as “fence-posts” and were inserted along the tumor boundaries, avoiding the PT, before tumor removal using the navigation system (fence-post catheter techniques). Cortical and subcortical MEPs were also monitored during resection of the tumor. Fence-post catheter techniques using a tractography integrated navigation system were used in 45 of 49 patients.

This technique enabled placement of the catheters, avoided the motor pathways, and allowed easier resection of the tumors. Tumors near the PT were resected using subcortical and cortical MEPs. The amplitudes of cortical MEPs after tumor removal were maintained at over 33 % of those obtained before resection.

Thirty-six patients showed obvious responses of subcortical MEPs at ≤20 mA. The degree of resection was gross total in 21 patients, subtotal in 21, and partial in seven. One month after surgery, only one patient showed worsened motor function.

Therefore, fence-post catheter techniques using a tractography-integrated navigation system and MEPs may contribute to preserving motor function after surgery for GBMs that are near the PT.

Modulation of the Cerebello-Thalamo-Cortical Network in Thalamic Deep Brain Stimulation for Tremor

Modulation of the Cerebello-Thalamo-Cortical Network in Thalamic Deep Brain Stimulation for Tremor- A Diffusion Tensor Imaging Study

Neurosurgery 75:657–670, 2014

Deep brain stimulation alleviates tremor of various origins. Several regions like the ventralis intermediate nucleus of thalamus, the caudal zona incerta, and the posterior subthalamic region are generally targeted. Previous work with fiber tractography has shown the involvement of the cerebello-thalamo-cortical network in tremor control.

OBJECTIVE: To report the results of a prospective trial in a group of patients with tremor who underwent post hoc tractographic analysis after treatment with traditional thalamic deep brain stimulation.

METHODS: A total of 11 patients (aged 64 6 17 years, 6 male) were enrolled (essential tremor [6], Parkinson tremor [3], and myoclonic tremor in myoclonus dystonia [2]). Patients received 1 (3 patients), 2 (7 patients), or 3 (1 patient) quadripolar electrodes. A 32-direction diffusion tensor magnetic resonance imaging sequence was acquired preoperatively. Tractography was processed postoperatively for evaluation and the dentato-rubro-thalamic tract (DRT) was individually tracked. Electrode positions were determined with helical computed tomography. Electric fields (EFs) were simulated according to individual stimulation parameters in a standardized atlas brain space (ICBMMNI 152).

RESULTS: Tremor was reduced in all patients (69.4% mean) on the global (bilateral) tremor score. Effective contacts were located inside or in proximity to the DRT. In moderate tremor reduction (2 patients), the EFs were centered on its anterior border. In good and excellent tremor reduction (9 patients), EFs focused on its center.

CONCLUSION: Deep brain stimulation of the cerebello-thalamo-cortical network reduces tremor. The DRT connects 3 traditional target regions for deep brain stimulation in tremor disease. Tractography techniques can be used to directly visualize the DRT and, therefore, optimize target definition in individual patients.

Intraoperative visualisation of language fascicles by diffusion tensor imaging-based tractography in glioma surgery

Intraop visualization language fascicles-3

Acta Neurochir (2013) 155:437–448

For gliomas, the goal of surgery is to maximise the extent of resection (EOR) while minimising the postoperative morbidity. The purpose of this study was to evaluate the benefits of a protocol developed for the surgical management of gliomas located in language areas, where tractography-integrated navigation was used in conjunction with direct electrical stimulations (DES).

Methods and materials The authors included ten patients suffering of gliomas located in language areas. The preoperative planning for multimodal navigation was done by integrating anatomical magnetic resonance images and subcortical pathway volumes generated by diffusion tensor imaging. Six white matter fascicles implicated in language functions were reconstructed in each patient, including fibres for phonological processing (i.e. the arcuate fasciculus), fibres for lexical-semantic processing (i.e. the inferior frontooccipital fasciculus, inferior longitudinal fasciculus and uncinate fasciculus), and two premotor fasciculi involved in the preparation of speech movements (the subcallosal medialis fasciculus and cortical fibres originating from the medial and lateral premotor areas). During surgery, language fascicles were identified by direct visualisation on tractography-integrated navigation images and by observing transient language inhibition after subcortical DES. Language deficits were evaluated preoperatively and postoperatively, and compared with the EOR.

Results Tractography was successfully performed in all patients, preoperatively demonstrating the relationships between the tumours to resect and the language fascicles to preserve from injury. With the use of the tractographyintegrated navigation system and intraoperative DES, language functions were preserved in all patients. The mean volumetric resection was 93.0±10.4 % of the preoperative tumour volume, with a gross total resection in 60 % of patients.

Conclusion The intraoperative combination of tractography and DES contributed to maximum safe resection of gliomas located in language areas.

Clinical Application of Motor Pathway Mapping Using Diffusion Tensor Imaging Tractography and Intraoperative Direct Subcortical Stimulation in Cerebral Glioma Surgery

Neurosurgery 71:1170–1184, 2012

Glioma surgery in eloquent areas remains a challenge because of the risk of postoperative motor deficits.

OBJECTIVE: To prospectively evaluate the efficiency of using a combination of diffusion tensor imaging (DTI) tractography functional neuronavigation and direct subcortical stimulation (DsCS) to yield a maximally safe resection of cerebral glioma in eloquent areas.

METHODS: A prospective cohort study was conducted in 58 subjects with an initial diagnosis of primary cerebral glioma within or adjacent to the pyramidal tract (PT). The white matter beneath the resection cavity was stimulated along the PT, which was visualized with DTI tractography. The intercept between the PT border and DsCS site was measured. The sensitivity and specificity of DTI tractography for PT mapping were evaluated. The efficiency of the combined use of both techniques on motor function preservation was assessed.

RESULTS: Postoperative analysis showed gross total resection in 40 patients (69.0%). Seventeen patients (29.3%) experienced postoperative worsening; 1-month motor deficit was observed in 6 subjects (10.3%). DsCS verified a high concordance rate with DTI tractography for PT mapping. The sensitivity and specificity of DTI were 92.6% and 93.2%, respectively. The intercepts between positive DsCS sites and imaged PTs were 2.0 to 14.7 mm (5.262.2 mm). The 6-month Karnofsky Performance Scale scores in 50 postoperative subjects were significantly increased compared with their preoperative scores.

CONCLUSION: DTI tractography is effective but not completely reliable in delineating the descending motor pathways. Integration of DTI and DsCS favors patient-specific surgery for cerebral glioma in eloquent areas.

Delineation of the Safe Zone in Surgery of Sylvian Insular Triangle

Neurosurgery 70[ONS Suppl 2]:ons290–ons299, 2012.DOI: 10.1227/NEU.0b013e3182315112

Surgery within the insula carries significant risk of morbidity, particularly hemiparesis, because of the difficulty in detecting the internal capsule boundaries.

OBJECTIVE: We analyzed the anatomy of the insula and identified landmarks anticipated to facilitate surgery for intrinsic insular lesions.

METHODS: Insular region anatomy was studied in 11 cadaveric brains harvested within 72 hours postmortem. MRI of the specimens was acquired using 3.0 T with T2-weighting and 25 directions of diffusion tensor imaging. Landmarks easily recognizable during surgery were identified on the surface of the insula. The interrelationships between surface landmarks and critical structures were analyzed.

RESULTS: The posterior inferior insular point (PIIP) and the upper central insular point (UCIP) were newly established as landmarks on the insula. The PIIP corresponded to the obvious bend in the posterior long insular gyrus. The UCIP is the meeting point between the central insular sulcus and superior peri-insular sulcus. The corticospinal tract was identified as a high-intensity area in the posterior limb of the internal capsule on T2-weighted imaging and its course confirmed with diffusion tensor imaging tractography. The corticospinal tract took a course deep to the posterosuperior insula on T2-weighted imaging, 4.8 mm from the UCIP and 6.2 mm from the PIIP.

CONCLUSION: The posterosuperior part of the insula forms the region at greatest risk to corticospinal tract injury. The PIIP and UCIP are crucial to understanding the relationship of the insula with the posterior limb of the internal capsule including the corticospinal tract.

KEY WORDS:

Accuracy of Diffusion Tensor Magnetic Resonance Imaging-Based Tractography for Surgery of Gliomas Near the Pyramidal Tract

Neurosurgery 70:283–294, 2012 DOI: 10.1227/NEU.0b013e31823020e6

Diffusion tensor (DT) imaging-based fiber tracking is a noninvasive magnetic resonance technique that can delineate the course of white matter fibers.

OBJECTIVE: To evaluate the accuracy and usefulness of this DT imaging-based fiber tracking for surgery in patients with gliomas near the pyramidal tract (PT).

METHODS: Subjects comprised 32 patients with gliomas near the PT. DT imagingbased fiber tracks of the PT were generated before and within 3 days after surgery in all patients. A tractography-integrated navigation system was used during the operation. Cortical and subcortical motor-evoked potentials (MEPs) were also monitored during resection to maximize the preservation of motor function. The threshold intensity for subcortical MEPs was examined by searching the stimulus points and changing the stimulus intensity. Minimum distance between the resection border and the illustrated PT was measured on postoperative tractography.

RESULTS: In all subjects, DT imaging-based tractography of the PT was successfully performed, preoperatively demonstrating the relationship between tumors and the PT. With the use of the tractography-integrated navigation system and intraoperative MEPs, motor function was preserved postoperatively in all patients. A significant correlation was seen between threshold intensity for subcortical MEPs and the distance between the resection border and PT on postoperative DT imaging.

CONCLUSION: DT imaging-based fiber tracking is a reliable and accurate method for mapping the course of subcortical PTs. Fiber tracking and intraoperative MEPs were useful for preserving motor function in patients with gliomas near the PT.

The motor-evoked potential threshold evaluated by tractography and electrical stimulation

J Neurosurg 111:785–795, 2009.DOI: 10.3171/2008.9.JNS08414

Object. To validate the corticospinal tract (CST) illustrated by diffusion tensor imaging, the authors used tractography-integrated neuronavigation and direct fiber stimulation with monopolar electric currents.
Methods. Forty patients with brain lesions adjacent to the CST were studied. During the operation, the motor responses (motor evoked potential [MEP]) elicited at the hand by the cortical stimulation to the hand motor area were continuously monitored, maintaining the consistent stimulus intensity (mean 15.1 ± 2.21 mA). During lesion resection, direct fiber stimulation was applied to elicit MEP (referred to as fiber MEP) to identify the CST functionally. The threshold intensity for the fiber MEP was determined by searching for the best stimulus point and changing the stimulus intensity. The minimum distance between the resection border and illustrated CST was measured on postoperative
isotropic images.
Results. Direct fiber stimulation demonstrated that tractography accurately reflected anatomical CST functioning. There were strong correlations between stimulus intensity for the fiber MEP and the distance between the CST and the stimulus points. The results indicate that the minimum stimulus intensity of 20, 15, 10, and 5 mA had stimulus points ~ 16, 13.2, 9.6, and 4.8 mm from the CST, respectively. The convergent calculation formulated 1.8 mA as the electrical threshold of the CST for the fiber MEP, which was much smaller than that of the hand motor area.
Conclusions. The investigators found that diffusion tensor imaging–based tractography is a reliable way to map the white matter connections in the entire brain in clinical and basic neuroscience applications. By combining these techniques, investigating the cortical-subcortical connections in the human CNS could contribute to elucidating the neural networks of the human brain and shed light on higher brain functions.