Language hemispheric dominance analyzed with magnetic resonance DTI: correlation with the Wada test

J Neurosurg 134:1703–1710, 2021

Language lateralization is a major concern in some patients with pharmacoresistant epilepsy who will face surgery; in these patients, hemispheric dominance testing is essential to avoid further complications. The Wada test is considered the gold standard examination for language localization, but is invasive and requires many human and material resources. Functional MRI and tractography with diffusion tensor imaging (DTI) have demonstrated that they could be useful for locating language in epilepsy surgery, but there is no evidence of the correlation between the Wada test and DTI MRI in language dominance.

METHODS The authors performed a retrospective review of patients who underwent a Wada test before epilepsy surgery at their institution from 2012 to 2017. The authors retrospectively analyzed fractional anisotropy (FA), number and length of fibers, and volume of the arcuate fasciculus and uncinate fasciculus, comparing dominant and nondominant hemispheres.

RESULTS Ten patients with temporal lobe epilepsy were reviewed. Statistical analysis showed that the mean FA of the arcuate fasciculus in the dominant hemisphere was higher than in the nondominant hemisphere (0.369 vs 0.329, p = 0.049). Also, the number of fibers in the arcuate fasciculus was greater in the dominant hemisphere (881.5 vs 305.4, p = 0.003). However, no differences were found in the FA of the uncinate fasciculus or number of fibers between hemispheres. The length of fibers of the uncinate fasciculus was longer in the dominant side (74.4 vs 50.1 mm, p = 0.05). Volume in both bundles was more prominent in the dominant hemisphere (12.12 vs 6.48 cm3, p = 0.004, in the arcuate fasciculus, and 8.41 vs 4.16 cm3, p = 0.018, in the uncinate fasciculus). Finally, these parameters were compared in patients in whom the seizure focus was situated in the dominant hemisphere: FA (0.37 vs 0.30, p = 0.05), number of fibers (114.4 vs 315.6, p = 0.014), and volume (12.58 vs 5.88 cm3, p = 0.035) in the arcuate fasciculus were found to be statistically significantly higher in the dominant hemispheres. Linear discriminant analysis of FA, number of fibers, and volume of the arcuate fasciculus showed a correct discrimination in 80% of patients (p = 0.024).

CONCLUSIONS The analysis of the arcuate fasciculus and other tract bundles by DTI could be a useful tool for language location testing in the preoperative study of patients with refractory epilepsy.

Deep brain stimulation for aggressiveness: long-term follow-up and tractography study of the stimulated brain areas

J Neurosurg 134:366–375, 2021

Initial studies applying deep brain stimulation (DBS) of the posteromedial hypothalamus (PMH) to patients with pathological aggressiveness have yielded encouraging results. However, the anatomical structures involved in its therapeutic effect have not been precisely identified. The authors’ objective was to describe the long-term outcome in their 7-patient series, and the tractography analysis of the volumes of tissue activated in 2 of the responders.

METHODS This was a retrospective study of 7 subjects with pathological aggressiveness. The findings on MRI with diffusion tensor imaging (DTI) in 2 of the responders were analyzed. The authors generated volumes of tissue activated according to the parameters used, and selected those volumes as regions of interest to delineate the tracts affected by stimulation.

RESULTS The series consisted of 5 men and 2 women. Of the 7 patients, 5 significantly improved with stimulation. The PMH, ventral tegmental area, dorsal longitudinal fasciculus, and medial forebrain bundle seem to be involved in the stimulation field.

CONCLUSIONS In this series, 5 of 7 medication-resistant patients with severe aggressiveness who were treated with bilateral PMH DBS showed a significant long-lasting improvement. The PMH, ventral tegmental area, dorsal longitudinal fasciculus, and medial forebrain bundle seem to be in the stimulation field and might be responsible for the therapeutic effect of DBS.

 

The Surgical White Matter Chassis: A Practical 3-Dimensional Atlas for Planning Subcortical Surgical Trajectories

Operative Neurosurgery 14:469–482, 2018

The imperative role of white matter preservation in improving surgical functional outcomes is now recognized. Understanding the fundamental white matter framework is essential for translating the anatomic and functional literature into practical strategies for surgical planning and neuronavigation.

OBJECTIVE: To present a 3-dimensional (3-D) atlas of the structural and functional scaffolding of human white matter—ie, a “Surgical White Matter Chassis (SWMC)”—that can be used as an organizational tool in designing precise and individualized trajectorybased neurosurgical corridors.

METHODS: Preoperative diffusion tensor imaging magnetic resonance images were obtained prior to each of our last 100 awake subcortical resections, using a clinically available 3.0 Tesla system. Tractography was generated using a semiautomated deterministic global seeding algorithm. Tract data were conceptualized as a 3-D modular chassis based on the 3 major fiber types, organized along median and paramedian planes, with special attention to limbic and neocortical association tracts and their interconnections.

RESULTS: We discuss practical implementation of the SWMC concept, and highlight its use in planning select illustrative cases. Emphasis has been given to developing practical understanding of the arcuate fasciculus, uncinate fasciculus, and vertical rami of the superior longitudinal fasciculus, which are often-neglected fibers in surgical planning.

CONCLUSION: A working knowledge of white matter anatomy, as embodied in the SWMC, is of paramount importance to the planning of parafascicular surgical trajectories, and can serve as a basis for developing reliable safe corridors, or modules, toward the goal of “zerofootprint” transsulcal access to the subcortical space.

 

 

The Superior Frontal Transsulcal Approach to the Anterior Ventricular System

OBJECTIVE: To explore the superior frontal sulcus (SFS) morphology, trajectory of the applied surgical corridor, and white matter bundles that are traversed during the superior frontal transsulcal transventricular approach.

METHODS: Twenty normal, adult, formalin-fixed cerebral hemispheres and 2 cadaveric heads were included in the study. The topography, morphology, and dimensions of the SFS were recorded in all specimens. Fourteen hemispheres were investigated through the fiber dissection technique whereas the remaining 6 were explored using coronal cuts. The cadaveric heads were used to perform the superior frontal transsulcal transventricular approach. In addition, 2 healthy volunteers underwent diffusion tensor imaging and tractography reconstruction studies.

RESULTS: The SFS was interrupted in 40% of the specimens studied and was always parallel to the interhemispheric fissure. The proximal 5 cm of the SFS (starting from the SFS precentral sulcus meeting point) were found to overlie the anterior ventricular system in all hemispheres. Five discrete white matter layers were identified en route to the anterior ventricular system (i.e., the arcuate fibers, the frontal aslant tract, the external capsule, internal capsule, and the callosal radiations). Diffusion tensor imaging studies confirmed the fiber tract architecture.

CONCLUSIONS: When feasible, the superior frontal transsulcal transventricular approach offers a safe and effective corridor to the anterior part of the lateral ventricle because it minimizes brain retraction and transgression and offers a wide and straightforward working corridor. Meticulous preoperative planning coupled with a sound microneurosurgical technique are prerequisites to perform the approach successfully

 

 

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.

 

Fiber tracking for temporal tumors

Distinct displacements of the optic radiation based on tumor location revealed using preoperative diffusion tensor imaging

J Neurosurg 124:1343–1352, 2016

Visual field defects (VFDs) due to optic radiation (OR) injury are a common complication of temporal lobe surgery. The authors analyzed whether preoperative visualization of the optic tract would reduce this complication by influencing the surgeon’s decisions about surgical approaches. The authors also determined whether white matter shifts caused by temporal lobe tumors would follow predetermined patterns based on the tumor’s topography.

Methods One hundred thirteen patients with intraaxial tumors of the temporal lobe underwent preoperative diffusion tensor imaging (DTI) fiber tracking. In 54 of those patients, both pre- and postoperative VFDs were documented using computerized perimetry. Brainlab’s iPlan 2.5 navigation software was used for tumor reconstruction and fiber visualization after the fusion of DTI studies with their respective magnetization-prepared rapid gradient-echo (MP-RAGE) images. The tracking algorithm was as follows: minimum fiber length 100 mm, fractional anisotropy threshold 0.1. The lateral geniculate body and the calcarine cortex were employed as tract seeding points. Shifts of the OR caused by tumor were visualized in comparison with the fiber tracking of the patient’s healthy hemisphere.

Results Temporal tumors produced a dislocation of the OR but no apparent fiber destruction. The shift of white matter tracts followed fixed patterns dependent on tumor location: Temporolateral tumors resulted in a medial fiber shift, and thus a lateral transcortical approach is recommended. Temporopolar tumors led to a posterior shift, always including Meyer’s loop; therefore, a pterional transcortical approach is recommended. Temporomesial tumors produced a lateral and superior shift; thus, a transsylvian-transcisternal approach will result in maximum sparing of the fibers. Temporocentric tumors also induced a lateral fiber shift. For those tumors, a transsylvian-transopercular approach is recommended. Tumors of the fusiform gyrus generated a superior (and lateral) shift; consequently, a subtemporal approach is recommended to avoid white matter injury. In applying the approaches recommended above, new or worsened VFDs occurred in 4% of the patient cohort. Total neurological and surgical morbidity were less than 10%. In 90% of patients, gross-total resection was accomplished.

Conclusions Preoperative visualization of the OR may help in avoiding postoperative VFDs.

High-Definition Fiber Tractography of the Human Brain: Neuroanatomical Validation and Neurosurgical Applications

Neurosurgery 71:430–453, 2012

High-definition fiber tracking (HDFT) is a novel combination of processing, reconstruction, and tractography methods that can track white matter fibers from cortex, through complex fiber crossings, to cortical and subcortical targets with subvoxel resolution.

OBJECTIVE: To perform neuroanatomical validation of HDFT and to investigate its neurosurgical applications.

METHODS: Six neurologically healthy adults and 36 patients with brain lesions were studied. Diffusion spectrum imaging data were reconstructed with a Generalized Q-Ball Imaging approach. Fiber dissection studies were performed in 20 human brains, and selected dissection results were compared with tractography.

RESULTS: HDFT provides accurate replication of known neuroanatomical features such as the gyral and sulcal folding patterns, the characteristic shape of the claustrum, the segmentation of the thalamic nuclei, the decussation of the superior cerebellar peduncle, the multiple fiber crossing at the centrum semiovale, the complex angulation of the optic radiations, the terminal arborization of the arcuate tract, and the cortical segmentation of the dorsal Broca area. From a clinical perspective, we show that HDFT provides accurate structural connectivity studies in patients with intracerebral lesions, allowing qualitative and quantitative white matter damage assessment, aiding in understanding lesional patterns of white matter structural injury, and facilitating innovative neurosurgical applications. High-grade gliomas produce significant disruption of fibers, and low-grade gliomas cause fiber displacement. Cavernomas cause both displacement and disruption of fibers.

CONCLUSION: Our HDFT approach provides an accurate reconstruction of white matter fiber tracts with unprecedented detail in both the normal and pathological human brain. Further studies to validate the clinical findings are needed.

Diffusion tensor imaging fiber tracking using navigated brain stimulation

Acta Neurochir (2012) 154:555–563. DOI 10.1007/s00701-011-1255-3

Navigated brain stimulation (NBS) is a newly evolving technique. In addition to its supposed purpose, e.g., preoperative mapping of the central region, little is known about its further use in neurosurgery. We evaluated the usefulness of diffusion tensor imaging fiber tracking (DTI-FT) based on NBS compared to conventional characterization of the seed region.

Methods We examined 30 patients with tumors in or close to the corticospinal tract (CST) using NBS with the Nexstim eXimia system. NBS was performed for motor cortex mapping, and DTI-FT was performed by three different clinicians using BrainLAB iPlan® Cranial 3.0.1 at two time points. Number of fibers, tract volume, aberrant tracts, and proximity to the tumor were compared between the two methods.

Results We recognized a higher number of fibers (1,298± 1,279 vs. 916±986 fibers; p<0.01), tract volume (23.0±15.3 vs. 18.3±14.0 cm3; p<0.01), and aberrant tracts (0.6±0.5 vs. 0.3±0.5 aberrant tracts/tracked CST; p<0.001) when the seed region was defined conventionally, while proximity of the tracts to the tumor did not differ. While NBS-based DTI-FT is independent of the planning clinician, conventional outlining of the seed region shows generally higher variability between investigators.

Conclusions Conventional DTI-FT showed significant differences between the two modalities, most likely because of the more specific definition of the seed region when DTI-FT is based on NBS. Moreover, NBS-aided DTI fiber tracking is user-independent and, therefore, a method for further standardization of DTI fiber tracking.