Full tractography for detecting the position of cranial nerves in preoperative planning for skull base surgery: technical note

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OBJECTIVE

Diffusion imaging tractography has allowed the in vivo description of brain white matter. One of its applications is preoperative planning for brain tumor resection. Due to a limited spatial and angular resolution, it is difficult for fiber tracking to delineate fiber crossing areas and small-scale structures, in particular brainstem tracts and cranial nerves. New methods are being developed but these involve extensive multistep tractography pipelines including the patient-specific design of multiple regions of interest (ROIs). The authors propose a new practical full tractography method that could be implemented in routine presurgical planning for skull base surgery.

METHODS

A Philips MRI machine provided diffusion-weighted and anatomical sequences for 2 healthy volunteers and 2 skull base tumor patients. Tractography of the full brainstem, the cerebellum, and cranial nerves was performed using the software DSI Studio, generalized-q-sampling reconstruction, orientation distribution function (ODF) of fibers, and a quantitative anisotropy–based generalized deterministic algorithm. No ROI or extensive manual filtering of spurious fibers was used. Tractography rendering was displayed in a tridimensional space with directional color code. This approach was also tested on diffusion data from the Human Connectome Project (HCP) database.

RESULTS

The brainstem, the cerebellum, and the cisternal segments of most cranial nerves were depicted in all participants. In cases of skull base tumors, the tridimensional rendering permitted the visualization of the whole anatomical environment and cranial nerve displacement, thus helping the surgical strategy.

CONCLUSIONS

As opposed to classical ROI-based methods, this novel full tractography approach could enable routine enhanced surgical planning or brain imaging for skull base tumors.

ABBREVIATIONS CISS = constructive interference steady state; CN = cranial nerve; FSL = FMRIB software library; HCP = Human Connectome Project; HDFT = high-definition fiber tracking; ODF = orientation distribution function; ROA = region of avoidance; ROI = region of interest.

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Article Information

Correspondence Timothée Jacquesson: University of Pittsburgh School of Medicine, University of Pittsburgh Medical Center, Pittsburgh, PA. timothee.jacquesson@neurochirurgie.fr.

INCLUDE WHEN CITING Published online April 19, 2019; DOI: 10.3171/2019.1.JNS182638.

Disclosures The authors report no conflict of interest concerning the materials or methods used in this study or the findings specified in this paper.

© AANS, except where prohibited by US copyright law.

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Figures

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    Study diagram. From a Philips MRI machine and using a dedicated acquisition protocol, we applied a full-brainstem tractography approach that included: distortion correction, ROA design, tumor segmentation if required, an ODF-based generalized deterministic algorithm, and tridimensional rendering.

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    Region of avoidance (ROA) design. The brainstem, the cerebellum, and skull base cisterns are identified on T2-weighted anatomical images (axial view, A), then a single ROI is drawn to include all of these on the orientation of distribution function (ODF) map (B) before being negated to create an ROA (C). Tumor segmentation was performed separately to add a second ROA if required. No ROI was used. Full tractography was initiated out of the ROA(s), which reduced the manual step of multiple ROI design. The final workspace of full tractography is displayed in an oblique tridimensional view (D). A = anterior; L = lateral; P = posterior; R = right. Figure is available in color online only.

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    Full-brainstem tractography of a healthy subject. These diffusion data, acquired on a Philips MRI machine, led to the reconstruction of much longer segments of cranial nerves (inferior and oblique views, respectively, A and B); for instance, the orbital portion of the optic nerve (ON) and oculomotor nerve (III) and the cavernous portion of the trigeminal nerve with its 3 branches (V1, V2, and V3). The trajectory of CN III was first slightly descending, probably due to its usual course within the vascular pinch of basilar termination arteries, and was then oblique anteriorly and laterally, before entering the orbit. The right abducens nerve (VI) was identified, as well as thin fibers circumventing the cerebral peduncles that corresponded to the trochlear nerve (IV). Cranial nerves that belong to the acoustic-facial bundle (VII-VIII) or lower cranial nerves (LN) can be distinguished. A few fibers of the olfactory nerve (Olf) can be found, although its emergence at the anterior perforating space is not seen. Some rootlets of the hypoglossal nerve at the preolivary sulcus are observed, as well as the ascending branch of the accessory nerve (XI). The mesencephalon was correctly reconstructed (superior view, C) unlike the medulla oblongata, in which ascending/descending fibers were missing. OT = optic tract. Figure is available in color online only.

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    Full-brainstem tractography magnification of the mesencephalon contents, the interpeduncular fossa, and the cerebellopontine angle. Full-brainstem tractography provided a unique insight into the true anatomy of the brainstem, the cerebellum, and cranial nerves. A sectional cut at the upper level of the mesencephalon allowed visualization of its gross architecture, including an oblique view of the cerebral peduncles (CPed) in violet, the ascending spinothalamic (STT) and descending corticospinal tracts in blue, colliculus nuclei (inferior colliculi, CI) in red, and fibers coursing anteriorly that could match with oculomotor nerves in green (superior view, A). The interpeduncular fossa (IPF) is well identified between the 2 cerebral peduncles (CPed) and the chiasma (meeting point of optic tracts and optic nerves) while the oculomotor nerves (III) emerge at the inferior edge of the triangle and the pituitary stalk (PS) dives anteriorly (anterior view, B). At the cerebellopontine angle, the acoustic-facial bundle (VII-VIII) and the lower cranial nerves (LN) emerge medial to the flocculus. Above, the trigeminal nerve courses anteriorly and divides into 3 branches (V1, V2, and V3). The abducens nerve (VI) crosses from the pontomedullary sulcus just medially to the trigeminal nerve. The facial nerve can be distinguished from the cochlear nerve (anterior view, C). The accessory nerve (XI) can also be distinguished from the glossopharyngeal (IX) and the vagus (X) nerves. A few fibers of the hypoglossal nerve (XII) can be seen at the preolivary sulcus. Figure is available in color online only.

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    Full-brainstem tractography of a large left vestibular schwannoma. In this case, a large right Koos-4 vestibular schwannoma compressing the brainstem and expanding the internal acoustic meatus, the acoustic-facial bundle (VII-VIII) was not identified on T2 CISS images. The trigeminal nerve seemed to be pushed superiorly and the lower cranial nerves (LN) displaced inferiorly (inferior view, A). Full-brainstem tractography allowed the visualization of the facial nerve at the anterior-superior side of the tumor (Video 1 and oblique view, B), while the lower cranial nerves (LN) were pushed inferiorly (superior view, C). Relationships with the trigeminal branches (V1, V2, and V3) and the abducens nerve (VI) were also detailed while the optic (ON) and oculomotor nerves (III) are well identified. Mes. = mesencephalon. Figure is available in color online only.

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    Full-brainstem tractography of a left petroclival meningioma. In this case, a left-sided upper petroclival meningioma, the oculomotor nerve was not clearly identified on standard T2-weighted images, even if the trigeminal and abducens nerves were thought to be crossing at the inferior medial tumor margin. Full-brainstem tractography depicted the oculomotor nerve (III) trajectory superiorly and the relationships between the tumor and CNs IV, V, and VI (inferior view, A). The 3 trigeminal branches (V1, V2, and V3) were recognized including their cavernous and foramen segments through the skull base, as well as the optic nerves including their intraorbital segment (ON). A few fibers of the trochlear nerve (IV) can be seen, circumventing the cerebral peduncles (lateral view, B). The acoustic-facial bundle (VII-VIII) and the lower cranial nerves (LN) were identified and distinguished from one another on both sides. The tridimensional rendering allowed us to mimic the surgical approach and choose the best one (oblique view, C). Figure is available in color online only.

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    Full-brainstem tractography approach applied on a healthy subject from the HCP database. These data from the HCP database allowed visualization of the tridimensional anatomy of the brainstem and the cerebellum. The 3 stages of the brainstem were adequately seen despite the few fibers of the cerebral peduncles (anterior and lateral views, respectively, A and B). The pyramidal shape of the cerebellum was reconstructed with many anatomical landmarks, such as: horizontal fissure (HF) and suboccipital fissure (SubOF), hemispheres, tonsils, median lobules (Cu = culmen; De = declive; Fo = folium; Py = pyramid; T = tonsils; Tu = tuber), flocculus, and cerebellopontine angle (posterior view, C). The culmen presented an expected ascending orientation. The third median cerebellar lobule (folium) was found as a groove between the cerebellar hemispheres. The cisternal portions of the oculomotor (III), trigeminal (V), acoustic-facial (VII-VIII), and lower cranial nerves (LN) were displayed. Conversely, the olfactory, trochlear, abducens, and hypoglossal nerves were not tracked. At the superior part, the optic tracts (OT) and nerves (ON) were identified on both sides of the chiasma. At the inferior part, the reliefs of the medulla and the spinal cord (Sc) were identified. Figure is available in color online only.

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    Limits of standard high-resolution T2-weighted MR images. A classical high-resolution T2-weighted sequence was used prior to the full tractography method, but the anatomical modifications induced by tumors (blue) hindered the identification of the full trajectory of the cranial nerves. In the case of a large vestibular schwannoma filling the internal acoustic meatus (A) the acoustic-facial bundle is not visualized (yellow arrow). In the case of a left upper petroclival meningioma (B), the oculomotor and abducens nerves are seen in part but not in their whole trajectory through the skull base (yellow arrow). Figure is available in color online only.

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