Antonio Meola

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

BACKGROUND 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. ABBREVIATIONS CN, cranial nerveCPT, corticopontine tractCST, corticospinal tractCTT, central tegmental tractDLF, dorsal longitudinal fasciculusHCP, Human Connectome ProjectML, medial lemniscusMLF, medial longitudinal fasciculusRST, rubrospinal tractSTT, spinothalamic tract.

The controversial existence of the human superior fronto-occipital fasciculus: Connectome-based tractographic study with microdissection validation.

The superior fronto‐occipital fasciculus (SFOF), a long association bundle that connects frontal and occipital lobes, is well‐documented in monkeys but is controversial in human brain. Its assumed role is in visual processing and spatial awareness. To date, anatomical and neuroimaging studies on human and animal brains are not in agreement about the existence, course, and terminations of SFOF. To clarify the existence of the SFOF in human brains, we applied deterministic fiber tractography to a template of 488 healthy subjects and to 80 individual subjects from the Human Connectome Project (HCP) and validated the results with white matter microdissection of post‐mortem human brains. The imaging results showed that previous reconstructions of the SFOF were generated by two false continuations, namely between superior thalamic peduncle (STP) and stria terminalis (ST), and ST and posterior thalamic peduncle. The anatomical microdissection confirmed this finding. No other fiber tracts in the previously described location of the SFOF were identified. Hence, our data suggest that the SFOF does not exist in the human brain. Hum Brain Mapp 36:4964–4971, 2015.

Population-averaged atlas of the macroscale human structural connectome and its network topology

Abstract A comprehensive map of the structural connectome in the human brain has been a coveted resource for understanding macroscopic brain networks. Here we report an expert‐vetted, population‐averaged atlas of the structural connectome derived from diffusion MRI data (N = 842). This was achieved by creating a high‐resolution template of diffusion patterns averaged across individual subjects and using tractography to generate 550,000 trajectories of representative white matter fascicles annotated by 80 anatomical labels. The trajectories were subsequently clustered and labeled by a team of experienced neuroanatomists in order to conform to prior neuroanatomical knowledge. A multi‐level network topology was then described using whole‐brain connectograms, with subdivisions of the association pathways showing small‐worldness in intra‐hemisphere connections, projection pathways showing hub structures at thalamus, putamen, and brainstem, and commissural pathways showing bridges connecting cerebral hemispheres to provide global efficiency. This atlas of the structural connectome provides representative organization of human brain white matter, complementary to traditional histologically‐derived and voxel‐based white matter atlases, allowing for better modeling and simulation of brain connectivity for future connectome studies.

Letter: Navigation-Linked Heads-Up Display in Intracranial Surgery: Early Experience

To the Editor: We read with great interest the paper entitled “NavigationLinked Heads-Up Display in Intracranial Surgery: Early Experience” by Mascitelli et al,1 recently published in your journal. The authors reported a series of 28 vascular lesions (aneurysms, arteriovenous malformations [AVMs], cavernous malformations), 53 oncologic lesions (intraparenchymal and skull-based) and 3 other lesions (abscess, cerebrospinal fluid leak, and a Teflon granuloma), treated with the support of Microscope-based Augmented Reality (MbAR). The reported series is particularly relevant when considering that a recent review on the applications of augmented reality (AR) in humans identified 18 studies published between 1996 and 2015, overall, including the treatment of 77 vascular lesions, 75 neoplastic lesions, and 43 other diseases.2 Despite the wide range of diseases in the present series, the list of surgical conditions amenable of AR-aided surgery is even longer, including acute and chronic hydrocephalus,3 neoplastic or non-neoplastic epileptogenic lesions,4 and brain hemorrhage.5 Currently, there are no prospective studies showing a significant difference between AR-aided surgeries vs the standard neuronavigation-guided procedures in terms of morbidity, mortality, and clinical effectiveness. Thus, at the moment, conclusions on the best AR system cannot be dragged. Nonetheless, the MbAR is not novel,6,7 and demonstrated several points of interest, but also some important limitations. Technically, MbAR consists of fiducial-based, optical coregistration of the microscope and patient’s head. The AR scene is created by overlapping the virtual content (provided by preoperative images), with the real content (provided by the microscope itself ), by means of a neuronavigation system. The final AR image is injected in the microscope eyepiece. Thus, the surgeon can comfortably see the virtual image on the natural axis of view connecting the surgical field with the surgeon’s eye. So, the MbAR setup overcomes an important source of error of other AR systems,8 namely the parallax error. That error occurs when different points of view of the same surgical target can be achieved by the surgeon’s eye and optic devices: when the operator’s point of view is the same as that of the real data source, there is no mismatch between what the surgeon sees and what the device actually captures. Conversely, when the surgeon and the data source have different points of view, there might be uncertainty, and potentially error, about the actual position of the target.8 Another advantage of the MbAR is the unpaired magnification respect to any other surgical visualization system. Anyway, when a macroscopic view of the surgical field is needed (ie, ventricular drain placement, initial steps of craniotomy), the use and setup of MbAR systems might be more cumbersome and time-consuming than traditional neuronavigation systems. A crucial limitation of the MbAR systems is the limited stereoscopic 3-D visualization of the AR scene. Ideally, the optimal AR scene would consist of a tridimensional virtual rendering of even complex geometric shapes, perfectly merging with a tridimensional view of the reality, without hiding the details of the surgical field itself. Conversely, the MbAR depicts the surgical target by means of dashed lines outlining the perimeter of the target itself in two dimensions. Additionally, the virtual component does not fully merge with the real component of the AR scene, but rather “pops out” of the scene itself. Unfortunately, the depth perception is critical for, at least, 3 main microsurgical task: first, for finding deep and/or small targets (ie, brain aneurysms)9; second, for treating complex lesions, as in the case of AVMs resection that requires a precise understanding of the relationship of the arterial feeders and the veins between them, and respect to the AVMnidus itself;10 third, to avoid critical structures close to the target, as in the case of skull base tumors surrounded by neurovascular structures7 or in the case of intraparenchymal tumors close to eloquent areas.11 Schematically, the limited stereoscopic visualization is due to 2 main reasons. First, the microscope captures a monoscopic bidimensional view of the surgical field and so, by definition, the tridimensional virtual image cannot merge with the real scene.8 Second, the representation of the virtual content, which might, at least in part, compensate for the monoscopic view, is still rudimental. Indeed, the depth perception can be improved by several visualization processing techniques.12 As an example, “Chromadepth” rendering, uses specific color-coding to represent distances following the visible light spectrum: near objects are red, while, as distance increases, objects are orange, yellow, green, and blue.13 Another example is the “Aerial Perspective” (aka “Fog” method), where colors became more transparent as the structures are deeper. Another important improvement for targeting surgical lesions, as well as for avoiding critical surrounding structures consists in adding procedural cues to the AR scene, such as the trajectory of the surgical instrument through the brain parenchyma and/or cisterns. This advancement can be theoretically achieved by fiducial-tracked surgical instruments, whose position can be determined respect to predetermined virtual trajectories, in a similar fashion to the traditional pointers of the neuronavigation systems. Alternatively, a much cheaper option consists in adding a series of isocentric, target-like, objects to the virtual content, allowing the surgeon adjusting the direction of the surgical instrument in order to center sequentially each of the target-like objects.11 Thus, as demonstrated in the present1 and previous studies,7,9,10,14 the MbAR is reliable and potentially useful for the initial “macroscopic” steps of brain surgeries (or just for treating superficial targets), including the skin incision, the craniotomy, the durotomy and the corticectomy, which can be

Magnetic Resonance Thermometry and Laser Interstitial Thermal Therapy for Brain Tumors

Recent technological advancements in intraoperative imaging are shaping the way for a new era in brain tumor surgery. Magnetic resonance thermometry has provided intraoperative real-time imaging feedback for safe and effective application of laser interstitial thermal therapy (LITT) in neuro-oncology. Thermal ablation has also established itself as a surgical option in epilepsy surgery and is currently used in spine oncology with promising results. This article reviews the principles and rationale as well as the clinical application of LITT for brain tumors. It also discusses the technical nuances of the current commercially available systems.

Stereotactic radiosurgery for jugular foramen schwannomas: an international multicenter study

OBJECTIVE For some jugular foramen schwannomas (JFSs), complete resection is possible but may be associated with significant morbidity. Stereotactic radiosurgery (SRS) is a minimally invasive alternative or adjunct to microsurgery for JFSs. The authors reviewed clinical and imaging outcomes of SRS for patients with these tumors. METHODS Nine participating centers of the International Gamma Knife Research Foundation identified 92 patients who underwent SRS between 1990 and 2013. Forty-one patients had prior subtotal microsurgical resection. The median interval between previous surgery and SRS was 15 months (range 0.5-144 months). Eighty-four patients had preexisting cranial nerve (CN) symptoms and signs. The median tumor volume was 4.1 cm3 (range 0.8-22.6 cm3), and the median margin dose was 12.5 Gy (range 10-18 Gy). Patients with neurofibromatosis were excluded from this study. RESULTS The median follow-up was 51 months (range 6-266 months). Tumors regressed in 47 patients, remained stable in 33, and progressed in 12. The progression-free survival (PFS) was 93% at 3 years, 87% at 5 years, and 82% at 10 years. In the entire series, only a dumbbell shape (extension extracranially via the jugular foramen) was significantly associated with worse PFS. In the group of patients without prior microsurgery (n = 51), factors associated with better PFS included tumor volume < 6 cm3 (p = 0.037) and non-dumbbell-shaped tumors (p = 0.015). Preexisting cranial neuropathies improved in 27 patients, remained stable in 51, and worsened in 14. The CN function improved after SRS in 12% of patients at 1 year, 24% at 2 years, 27% at 3 years, and 32% at 5 years. Symptomatic adverse radiation effects occurred in 7 patients at a median of 7 months after SRS (range 5-38 months). Six patients underwent repeat SRS at a median of 64 months (range 44-134 months). Four patients underwent resection at a median of 14 months after SRS (range 8-30 months). CONCLUSIONS Stereotactic radiosurgery proved to be a safe and effective primary or adjuvant management approach for JFSs. Long-term tumor control rates and stability or improvement in CN function were confirmed.

Improved Accuracy of Diffusion MRI Tractography Using Topology-Informed Pruning (TIP)

Diffusion MRI fiber tracking provides a non-invasive method for mapping the trajectories of human brain connections, but its false connection problem has been a major challenge. This study introduces topology-informed pruning (TIP), a method that improves the tractography of a target fiber bundle using its own topology information. TIP identifies singular tracts and eliminates them to improve the tracking accuracy. This method was applied to a tractography study with diffusion MRI data collected using two different diffusion sampling schemes (single-shell and grid). The accuracy of the tractography was evaluated by a team of 6 neuroanatomists in a blinded setting to examine whether TIP could improve the accuracy of tractography. The results showed that TIP achieved an average accuracy improvement of 11.93% in the single-shell scheme and 3.47% in the grid scheme. The improvement is significantly different from a random pruning (p-value < 0.001). The diagnostic agreement between TIP and neuroanatomists was comparable to the agreement between neuroanatomists. The proposed TIP algorithm can be used to automatically clean up noisy fibers in deterministic tractography, with a potential to confirm the existence of a fiber connection in basic neuroanatomical studies or clinical neurosurgical planning.Diffusion MRI fiber tracking provides a non-invasive method for mapping the trajectories of human brain connections, but its false connection problem has been a major challenge. This study introduces topology-informed pruning (TIP), a method that automatically identifies singular tracts and eliminates them to improve the tracking accuracy. The accuracy of the tractography with and without TIP was evaluated by a team of 6 neuroanatomists in a blinded setting to examine whether TIP could improve the accuracy. The results showed that TIP improved the tracking accuracy by 11.93% in the single-shell scheme and by 3.47% in the grid scheme. The improvement is significantly different from a random pruning (p-value < 0.001). The diagnostic agreement between TIP and neuroanatomists was comparable to the agreement between neuroanatomists. The proposed TIP algorithm can be used to automatically clean up noisy fibers in deterministic tractography, with a potential to confirm the existence of a fiber connection in basic neuroanatomical studies or clinical neurosurgical planning.

Bilateral Vestibular Schwannomas in Neurofibromatosis Type 2

Vestibular Schwannomas in Neurofibromatosis Type 2 A 32-year-old man with a family history of neurofibromatosis type 2 presented with balance difficulties and hearing loss. Magnetic resonance imaging revealed bilateral vestibular schwannomas.

Automatic Removal of False Connections in Diffusion MRI Tractography Using Topology-Informed Pruning (TIP)

Diffusion MRI fiber tracking provides a non-invasive method for mapping the trajectories of human brain connections, but its false connection problem has been a major challenge. This study introduces topology-informed pruning (TIP), a method that automatically identifies singular tracts and eliminates them to improve the tracking accuracy. The accuracy of the tractography with and without TIP was evaluated by a team of 6 neuroanatomists in a blinded setting to examine whether TIP could improve the accuracy. The results showed that TIP improved the tracking accuracy by 11.93% in the single-shell scheme and by 3.47% in the grid scheme. The improvement is significantly different from a random pruning (p value < 0.001). The diagnostic agreement between TIP and neuroanatomists was comparable to the agreement between neuroanatomists. The proposed TIP algorithm can be used to automatically clean-up noisy fibers in deterministic tractography, with a potential to confirm the existence of a fiber connection in basic neuroanatomical studies or clinical neurosurgical planning.

Commentary: Peritumoral Edema/Tumor Volume Ratio: A Strong Survival Predictor for Posterior Fossa Metastases

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