Anterior transtemporal endoscopic selective amygdalohippocampectomy

Acta Neurochirurgica (2022) 164:2841–2849

Selective amygdalohippocampectomy (SelAH) is one of the most common surgical treatments for mesial temporal sclerosis. Microsurgical approaches are associated with the risk of cognitive and visual deficits due to damage to the cortex and white matter (WM) pathways. Our objective is to test the feasibility of an endoscopic approach through the anterior middle temporal gyrus (aMTG) to perform a SelAH.

Methods Virtual simulation with MRI scans of ten patients (20 hemispheres) was used to identify the endoscopic trajectory through the aMTG. A cadaveric study was performed on 22 specimens using a temporal craniotomy. The anterior part of the temporal horn was accessed using a tubular retractor through the aMTG after performing a 1.5 cm corticectomy at 1.5 cm posterior to the temporal pole. Then, an endoscope was introduced. SeIAH was performed in each specimen. The specimens underwent neuronavigation-assisted endoscopic SeIAH to confirm our surgical trajectory. WM dissection using Klingler’s technique was performed on five specimens to assess WM integrity.

Results This approach allowed the identification of collateral eminence, lateral ventricular sulcus, choroid plexus, inferior choroidal point, amygdala, hippocampus, and fimbria. SelAH was successfully performed on all specimens, and CT neuronavigation confirmed the planned trajectory. WM dissection confirmed the integrity of language pathways and optic radiations.

Conclusions Endoscopic SelAH through the aMTG can be successfully performed with a corticectomy of 15 mm, presenting a reduced risk of vascular injury and damage to WM pathways. This could potentially help to reduce cognitive and visual deficits associated with SelAH.

Microsurgical anatomy of the sagittal stratum

Acta Neurochirurgica (2019) 161:2319–2327

The sagittal stratum (SS) is a critical neural crossroad traversed by several white matter tracts that connect multiple areas of the ipsilateral hemisphere. Scant information about the anatomical organization of this structure is available in literature. The goal of this study was to provide a detailed anatomical description of the SS and to discuss the functional implications of the findings when a surgical approach through this structure is planned.

Methods Five formalin-fixed human brains were dissected under the operating microscope by using the fiber dissection technique originally described by Ludwig and Klingler.

Results The SS is a polygonal crossroad of associational fibers situated deep on the lateral surface of the hemisphere, medial to the arcuate/superior longitudinal fascicle complex, and laterally to the tapetal fibers of the atrium. It is organized in three layers: a superficial layer formed by the middle and inferior longitudinal fascicles, a middle layer corresponding to the inferior frontooccipital fascicle, and a deep layer formed by the optic radiation, intermingled with fibers of the anterior commissure. It originates posteroinferiorly to the inferior limiting sulcus of the insula, contiguous with the fibers of the temporal stem, and ends into the posterior temporo-occipito-parietal cortex.

Conclusion The white matter fiber dissection reveals the tridimensional architecture of the SS and the relationship between its fibers. A detailed understanding of the anatomy of the SS is essential to decrease the operative risks when a surgical approach within this area is undertaken.

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 Impact of Intracranial Tumor Proximity to White Matter Tracts on Morbidity and Mortality

Neurosurgery 80:193–200, 2017

Using difusion tensor imaging (DTI) in neurosurgical planning allows identification of white matter tracts and has been associated with a reduction in postoperative functional deficits.
OBJECTIVE: This study explores the relationship between the lesion-to-tract distance (LTD) and postoperative morbidity and mortality in patients with brain tumors in order to evaluate the role of DTI in predicting postoperative outcomes.

METHODS: Adult patients with brain tumors (n = 60) underwent preoperative DTI. Three major white matter pathways (superior longitudinal fasciculi [SLF], cingulum, and corticospinal tract) were identified using DTI images, and the shortest LTD was measured for each tract. Postoperative morbidity and mortality information was collected from electronic medical records.

RESULTS: The ipsilesional corticospinal tract LTD and left SLF LTD were significantly associated with the occurrence rate of total postoperative motor (P = .018) and language (P < .001) deficits, respectively. The left SLF LTD was also significantly associated with the occurrence rate of new postoperative language deficits (P = .003), and the LTD threshold that best predicted this occurrence was 1 cm (P < .001). Kaplan–Meier log-rank survival analyses in patients having high-grade tumors demonstrated a significantly higher mortality for patients with a left SLF LTD <1 cm (P = .01).

CONCLUSION: Measuring tumor proximity to major white matter tracts using DTI can inform clinicians of the likelihood of postoperative functional deficits. A distance of 1 cm or less from eloquent white matter structures most significantly predicts the occurrence of new deficits with current surgical and imaging techniques.


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.

Frontal cortico-subcortical functional anatomy

Subcortical surgical anatomy of the lateral frontal region

J Neurosurg 117:1053–1069, 2012

Recent neuroimaging and surgical results support the crucial role of white matter in mediating motor and higher-level processing within the frontal lobe, while suggesting the limited compensatory capacity after damage to subcortical structures. Consequently, an accurate knowledge of the anatomofunctional organization of the pathways running within this region is mandatory for planning safe and effective surgical approaches to different diseases. The aim of this dissection study was to improve the neurosurgeon’s awareness of the subcortical anatomofunctional architecture for a lateral approach to the frontal region, to optimize both resection and postoperative outcome.

Methods. Ten human hemispheres (5 left, 5 right) were dissected according to the Klingler technique. Proceeding lateromedially, the main association and projection tracts as well as the deeper basal structures were identified. The authors describe the anatomy and the relationships among the exposed structures in both a systematic and topographical surgical perspective. Structural results were also correlated to the functional responses obtained during resections of infiltrative frontal tumors guided by direct cortico-subcortical electrostimulation with patients in the awake condition.

Results. The eloquent boundaries crucial for a safe frontal lobectomy or an extensive lesionectomy are as follows: 1) the motor cortex; 2) the pyramidal tract and premotor fibers in the posterior and posteromedial part of the surgical field; 3) the inferior frontooccipital fascicle and the superior longitudinal fascicle posterolaterally; and 4) underneath the inferior frontal gyrus, the head of the caudate nucleus, and the tip of the frontal horn of the lateral ventricle in the depth.

Conclusions. Optimization of results following brain surgery, especially within the frontal lobe, requires a perfect knowledge of functional anatomy, not only at the cortical level but also with regard to subcortical white matter connectivity.

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 Reveals Supplementary Lesions to Frontal White Matter in Idiopathic Normal Pressure Hydrocephalus

Neurosurgery 68:1586–1593, 2011 DOI: 10.1227/NEU.0b013e31820f3401

Idiopathic normal-pressure hydrocephalus (INPH) is associated with white matter lesions, but the extent and severity of the lesions do not cohere with symptoms or improvement after shunting, implying the presence of further, yet undisclosed, injuries to white matter in INPH.

OBJECTIVE: To apply diffusion tensor imaging (DTI) to explore white matter lesions in patients with INPH before and after drainage of cerebrospinal fluid (CSF).

METHODS: Eighteen patients and 10 controls were included. DTI was performed in a 1.5T MRI scanner before and after 3-day drainage of 400 mL of CSF. Regions of interest included corpus callosum, capsula interna, frontal and lateral periventricular white matter, and centrum semiovale. White matter integrity was quantified by assessing fractional anisotropies (FA) and apparent diffusion coefficients (ADC), comparing them between patients and controls and between patients before and after drainage. The significance level corresponded to .05 (Bonferroni corrected).

RESULTS: Decreased FA in patients was found in 3 regions (P < .002, P < .001, and P < .001) in anterior frontal white matter, whereas elevated ADC was found in genu corpus callosum (P < .001) and areas of centrum semiovale associated with the precentral gyri (P < .002). Diffusion patterns in these areas did not change after drainage.

CONCLUSION: DTI reveals subtle injuries—interpreted as axonal loss and gliosis—to anterior frontal white matter where high-order motor systems between frontal cortex and basal ganglia travel, further supporting the notion that motor symptoms in INPH are caused by a chronic ischemia to the neuronal systems involved in the planning processes of movements.

Microsurgical anatomy of the temporal stem: clinical relevance and correlations with diffusion tensor imaging fiber tracking

J Neurosurg 112:1033–1038, 2010. (DOI: 10.3171/2009.6.JNS08132)

The authors used a fiber dissection technique to describe the temporal stem and explain the tendency of malignant tumors to spread within both the frontal and temporal lobes. The authors focused on the morphological characteristics and course of various fasciculi of the temporal stem, including the uncinate fascicle, occipitofrontal fascicle, anterior commissure, loop of the optic radiations (Meyer loop), and the ansa peduncularis.

Methods. Eight previously frozen, formalin-fixed human brains were dissected under an operating microscope using the fiber dissection technique described by Klingler. Lateral, inferior, and medial approaches were made. Crosssectional 3D MR images obtained in 10 patients without brain lesions demonstrated that fibers of the temporal stem, which were intermingled together in various ways, curved laterally within the basal forebrain. Various pathological entities affecting the temporal stem are described and discussed.

Results. The uncinate fascicle has 3 portions: a ventral extension, an intermediary segment called the isthmus, and a dorsal segment. The inferior occipitofrontal fasciculus is a layer of more superficial white matter that appeared to be superior to the uncinate fasciculus. A short ventral portion of the radiations of the corpus callosum was sometimes noted to run ventrally to enter the temporal stem and to reach both temporal lobes.

Conclusions. To the authors’ knowledge, a detailed anatomy of the temporal stem has not been previously described in the literature. The unique anatomy of the temporal stem provides a route for tumor spread between the frontal and temporal lobes.

Microsurgical anatomy of the ventral callosal radiations: new destination, correlations with diffusion tensor imaging fiber-tracking, and clinical relevance

J Neurosurg 112:512–519, 2010.DOI: 10.3171/2009.6.JNS081712

In the current literature, there is a lack of a detailed map of the origin, course, and connections of the ventral callosal radiations of the human brain.

Methods. The authors used an older dissection technique based on a freezing process as well as diffusion tensor imaging to investigate this area of the human brain.

Results. The authors demonstrated interconnections between areas 11, 12, and 25 for the callosal radiations of the trunk and rostrum of the corpus callosum; between areas 9, 10, and 32 for the genu; and between areas 6, 8, and 9 for the ventral third of the body. The authors identified new ventral callosal connections crossing the rostrum between both temporal poles and coursing within the temporal stem, and they named these connections the “callosal radiations of Peltier.” They found that the breadth of the callosal radiations slightly increases along their course from the rostrum to the first third of the body of the corpus callosum.

Conclusions. The fiber dissection and diffusion tensor imaging techniques are complementary not only in their application to the study of the commissural system in the human brain, but also in their practical use for diagnosis and surgical planning. Further investigations, neurocognitive tests, and other contributions will permit elucidation of the functional relevance of the newly identified callosal radiations in patients with disease involving the ventral corpus callosum.

Tract-specific analysis of white matter pathways in healthy subjects: a pilot study using diffusion tensor MRI

Neuroradiology (2009) 51:831–840. DOI 10.1007/s00234-009-0580-1

To date, very scant data is available regarding normal diffusion properties of white matter (WM) fibers. The present study aimed to initiate the establishment of a database of normal diffusion tensor metrics of cerebral WM fibers, including the uncinate fasciculus (UF), posterior cingulum (PC), fornix, and corticospinal tract (CST) for healthy adults using tract-specific analysis by diffusion tensor tractography (DTT).We also attempted to clarify whether age and laterality exerted any effects on this study group.

Methods DTT of WM fibers were generated for 100 healthy subjects, then mean diffusivity (MD) and fractional anisotropy (FA) of the tracts were measured. Pearson correlation analysis was used to evaluate age relationships. Paired t testing was used to compare hemispheric asymmetry. Interobserver correlation tests were also performed.

Results Our results showed FA values for UF (right, 0.42±0.03; left, 0.40±0.03), PC (0.51±0.06, 0.52±0.06), fornix (0.37±0.06, 0.38±0.06), CST (0.70±0.06, 0.69±0.07), and MD values for UF (0.81±0.03, 0.82±0.04), PC (0.72±0.03, 0.72±0.04), fornix (1.86±0.32, 1.94±0.37), and CST (0.72±0.03, 0.74±0.04). We identified a significant positive

correlation between age and MD in the right UF and bilateral fornices, and a negative correlation between age and FA in bilateral fornices. Hemispheric asymmetry was observed in FA of UF (right>left) and MD of CST (left>right).

Conclusions The results constitute a normative dataset for diffusion parameters of four WM tracts that can be used to identify, characterize, and establish the significance of changes in diseases affecting specific tracts.

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