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Alexander S. G. Micko, Adelheid Wöhrer, Stefan Wolfsberger and Engelbert Knosp

OBJECT

An important prognostic factor for the surgical outcome and recurrence of a pituitary adenoma is its invasiveness into parasellar tissue, particularly into the space of the cavernous sinus (CS). The aims of this study were to reevaluate the existing parasellar classifications using an endoscopic technique and to evaluate the clinical and radiological outcomes associated with each grade.

METHODS

The authors investigated 137 pituitary macroadenomas classified radiologically at least on one side as Grade 1 or higher (parasellar extension) and correlated the surgical findings using an endoscopic technique, with special reference to the invasiveness of the tumor into the CS. In each case, postoperative MRI was performed to evaluate the gross-total resection (GTR) rate and the rate of endocrinological remission (ER) in functioning adenomas.

RESULTS

The authors found a 16% rate of CS invasion during surgery for these macroadenomas. Adenomas radiologically classified as Grade 1 were found to be invasive in 1.5%, and the GTR/ER rate was 83%/88%. For Grade 2 adenomas, the rate of invasion was 9.9%, and the GTR/ER rate was 71%/60%. For Grade 3 adenomas, the rate of invasion was 37.9%, and the GTR/ER rate was 75%/33%. When the superior compartment of the CS (Grade 3A) was involved, the authors found a rate of invasion that was lower (p < 0.001) than that when the inferior compartment was involved (Grade 3B). The rate of invasion in Grade 3A adenomas was 26.5% with a GTR/ER rate of 85%/67%, whereas for Grade 3B adenomas, the rate of surgically observed invasion was 70.6% with a GTR/ER rate of 64%/0%. All of the Grade 4 adenomas were invasive, and the GTR/ER rate was 0%.

A comparison of microscopic and endoscopic techniques revealed no difference in adenomas with Grade 1 or 4 parasellar extension. In Grade 2 adenomas, however, the CS was found by the endoscopic technique to be invaded in 9.9% and by microscopic evaluation to be invaded in 88% (p < 0.001); in Grade 3 adenomas, the difference was 37.9% versus 86%, respectively (p = 0.002). Grade 4 adenomas had a statistically significant lower rate of GTR than those of all the other grades. In case of ER only, Grade 1 adenomas had a statistically significant higher rate of remission than did Grade 3B and Grade 4 adenomas.

CONCLUSIONS

The proposed classification proved that with increasing grades, the likelihood of surgically observed invasion rises and the chance of GTR and ER decreases. The direct endoscopic view confirmed the low rate of invasion of Grade 1 adenomas but showed significantly lower rates of invasion in Grade 2 and 3 adenomas than those previously found using the microscopic technique. In cases in which the intracavernous internal carotid artery was encased (Grade 4), all the adenomas were invasive and the GTR/ER rate was 0%/0%. The authors suggest the addition of Grades 3A and 3B to distinguish the strikingly different outcomes of adenomas invading the superior CS compartments and those invading the inferior CS compartments.

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Stefan Wolfsberger, Ahmed Ba-Ssalamah, Katja Pinker, Vladimír Mlynárik, Thomas Czech, Engelbert Knosp and Siegfried Trattnig

Object

The aim of this study was to determine the value of high-field magnetic resonance (MR) imaging for diagnosis and surgery of sellar lesions.

Methods

High-field MR images were obtained using a 3-tesla unit with emphasis on sellar and parasellar structures in 21 patients preoperatively to delineate endo-, supra-, and parasellar anatomical structures. Special attention was given to the medial border of the cavernous sinus and possible invasion of a sellar tumor therein, and to assessing the application of high-resolution images during intraoperative neuronavigation. The 3-tesla MR images were compared with the standard MR images already obtained and with intraoperative findings.

Anatomical structures were studied in all 42 cavernous sinuses; in 32 of them comparisons with intraoperative findings were possible. The medial cavernous sinus border was rated intact in 53% on standard MR images, in 72% on 3-tesla MR images, and in 81% intraoperatively. With a positive correlation to surgical findings on 84% of 3-tesla MR images compared with 59% of standard MR images, a sensitivity of 83% compared with 67%, and a specificity of 84% compared with 58% (p = 0.016, McNemar test), 3-tesla MR imaging was superior for predicting tumor invasion through the medial cavernous sinus border. Although no difference was noted in delineation of the medial, superior, and inferior compartments, there was a better delineation of the lateral cavernous sinus compartment with 3-tesla MR imaging. This compartment was clearly visible on 40 sides (95%) on 3-tesla MR images compared with 34 sides (81%) on standard MR images. Identification of the cavernous sinus segments of the third, fourth, fifth (V1 and V2), and sixth cranial nerves was improved using high-resolution 3-tesla imaging compared with standard MR imaging. A mean of four cranial nerves was found as hypo-intense spots (range two–five spots) on 3-tesla MR imaging compared with a mean of three (range zero–four spots) on standard MR imaging. After addition of contrast agents, the anterior pituitary gland was found to be highly intense on 78% of T1-weighted three-dimensional magnetization-prepared rapid acquisition gradient-echo (MPRAGE) 3-tesla MR images compared with 73% of standard T1-weighted MR images. The optochiasmatic system displayed increased intensity on pre-contrast T1-weighted MPRAGE 3-tesla compared with standard T1-weighted MR images; it was hyperintense on 76% of 3-tesla compared with 15% of standard MR images, which was helpful for its delineation from suprasellar pituitary and tumor structures. Intraoperative navigation guided by fusion of 3-tesla MR images and computerized tomography (CT) scans was performed in seven patients. Whereas CT scanning was used during the transsphenoidal approach to depict the nasal bone structures, 3-tesla MR imaging was particularly useful for the visualization of parasellar tumor extension during microsurgical and/or endoscopic resection.

Conclusions

Due to its higher resolution, 3-tesla MR imaging was found to be superior to standard MR imaging for the delineation of parasellar anatomy and tumor infiltration of the cavernous sinus, and this modality provided improved imaging for intraoperative navigation.

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Garnette R. Sutherland, Sanju Lama, Liu Shi Gan, Stefan Wolfsberger and Kourosh Zareinia

Object

It has been over a decade since the introduction of the da Vinci Surgical System into surgery. Since then, technology has been advancing at an exponential rate, and newer surgical robots are becoming increasingly sophisticated, which could greatly impact the performance of surgery. NeuroArm is one such robotic system.

Methods

Clinical integration of neuroArm, an MR-compatible image-guided robot, into surgical procedure has been developed over a prospective series of 35 cases with varying pathology.

Results

Only 1 adverse event was encountered in the first 35 neuroArm cases, with no patient injury. The adverse event was uncontrolled motion of the left neuroArm manipulator, which was corrected through a rigorous safety review procedure. Surgeons used a graded approach to introducing neuroArm into surgery, with routine dissection of the tumor-brain interface occurring over the last 15 cases. The use of neuroArm for routine dissection shows that robotic technology can be successfully integrated into microsurgery. Karnofsky performance status scores were significantly improved postoperatively and at 12-week follow-up.

Conclusions

Surgical robots have the potential to improve surgical precision and accuracy through motion scaling and tremor filters, although human surgeons currently possess superior speed and dexterity. Additionally, neuroArm's workstation has positive implications for technology management and surgical education. NeuroArm is a step toward a future in which a variety of machines are merged with medicine.

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Andrej Šteňo, A. John Popp, Stefan Wolfsberger, Vít'azoslav Belan and Juraj Šteňo

Persisting embryonal infundibular recess (PEIR) is a rare anomaly of the third ventricular floor that has an unclear pathogenesis. In all 7 previously described cases, PEIR was present in adult patients and was invariably associated with hydrocephalus and, in 4 reported cases, with an empty sella. These associated findings led to speculations about the role of increased intraventricular pressure in the development of PEIR.

In the present case, PEIR was found in a 24-year-old man without the presence of hydrocephalus or empty sella. Disorders of pituitary function had been present since childhood. Magnetic resonance imaging revealed a cystic expansion in an enlarged sella turcica. A communication between the third ventricle and the sellar cyst was suspected but not apparent. During transcranial surgery, the connection was confirmed. Later, higher-quality MR imaging investigations clearly showed a communication between the third ventricle and the sellar cyst through a channel in the tubular pituitary stalk. This observation and knowledge about the embryology of this region suggests that PEIR may be a developmental anomaly caused by failure of obliteration of the distal part of primary embryonal diencephalic evagination. Thus, PEIR is an extension of the third ventricular cavity into the sella.

Although PEIR is a rare anomaly, it is important to identify when planning a procedure on cystic lesions of the sella. Because attempts at removal using the transsphenoidal approach would lead to a communication between the third ventricle and the nasal cavity, a watertight reconstruction of the sellar floor is necessary.

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Georg Widhalm, Stefan Wolfsberger, Matthias Preusser, Ingeborg Fischer, Adelheid Woehrer, Joerg Wunderer, Johannes A. Hainfellner and Engelbert Knosp

Object

In residual nonfunctioning pituitary adenomas, reliable prognostic parameters indicating probability of tumor progression are needed. The Ki 67 expression/MIB-1 labeling index (LI) is considered to be a promising candidate factor. The aim in the present study was to analyze the clinical usefulness of MIB-1 LI for prognosis of tumor progression.

Methods

The authors studied a cohort of 92 patients with nonfunctioning pituitary adenomas. Based on sequential postoperative MR images, patients were classified as tumor free (51 patients) or as harboring residual tumor (41 individuals). The residual tumor group was further subdivided in groups with stable residual tumors (14 patients) or progressive residual tumors (27 patients). The MIB-1 LI was assessed in tumor specimens obtained in all patients, and statistical comparisons of MIB-1 LI of the various subgroups were performed.

Results

. The authors found no significant difference of MIB-1 LI in the residual tumor group compared with the tumor-free group. However, MIB-1 LI was significantly higher in the progressive residual tumor group, compared with the stable residual tumor group. Additionally, the time period to second surgery was significantly shorter in residual adenomas showing an MIB-1 LI > 3%.

Conclusions

The data indicate that MIB-1 LI in nonfunctioning pituitary adenomas is a clinically useful prognostic parameter indicating probability of progression of postoperative tumor remnants. The MIB-1 LI may be helpful in decisions of postoperative disease management (for example, frequency of radiographic intervals, planning for reoperation, radiotherapy, and/or radiosurgery).

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Matthias Millesi, Barbara Kiesel, Adelheid Woehrer, Johannes A. Hainfellner, Klaus Novak, Mauricio Martínez-Moreno, Stefan Wolfsberger, Engelbert Knosp and Georg Widhalm

Object

Subtotal resection (STR) of spinal tumors can result in tumor recurrence. Currently, no clinically reliable marker is available for intraoperative visualization of spinal tumor tissue. Protoporphyrin IX (PpIX) fluorescence induced by 5-aminolevulinic acid (5-ALA) is capable of visualizing malignant gliomas. Fluorescence-guided resections of malignant cerebral gliomas using 5-ALA have resulted in an increased rate of complete tumor removal. Recently, the application of 5-ALA has also been described in the first cases of spinal tumors. Therefore, the aim of this observational study was to systematically investigate 5-ALA–induced fluorescence characteristics in different spinal tumor entities.

Methods

Three hours before the induction of anesthesia, 5-ALA was administered to patients with different intra- and extradural spinal tumors. In all patients a neurosurgical resection or biopsy of the spinal tumor was performed under conventional white-light microscopy. During each surgery, the presence of PpIX fluorescence was additionally assessed using a modified neurosurgical microscope. At the end of an assumed gross-total resection (GTR) under white-light microscopy, a final inspection of the surgical cavity of fluorescing intramedullary tumors was performed to look for any remaining fluorescing foci. Histopathological tumor diagnosis was established according to the current WHO classification.

Results

Fifty-two patients with 55 spinal tumors were included in this study. Resection was performed in 50 of 55 cases, whereas 5 of 55 cases underwent biopsy. Gross-total resection was achieved in 37 cases, STR in 5, and partial resection in 8 cases. Protoporphyrin IX fluorescence was visible in 30 (55%) of 55 cases, but not in 25 (45%) of 55 cases. Positive PpIX fluorescence was mainly detected in ependymomas (12 of 12), meningiomas (12 of 12), hemangiopericytomas (3 of 3), and in drop metastases of primary CNS tumors (2 of 2). In contrast, none of the neurinomas (8 of 8), carcinoma metastases (5 of 5), and primary spinal gliomas (3 of 3; 1 pilocytic astrocytoma, 1 WHO Grade II astrocytoma, 1 WHO Grade III anaplastic oligoastrocytoma) revealed PpIX fluorescence. It is notable that residual fluorescing tumor foci were detected and subsequently resected in 4 of 8 intramedullary ependymomas despite assumed GTR under white-light microscopy.

Conclusions

In this study, 5-ALA–PpIX fluorescence was observed in spinal tumors, especially ependymomas, meningiomas, hemangiopericytomas, and drop metastases of primary CNS tumors. In cases of intramedullary tumors, 5-ALA–induced PpIX fluorescence is a useful tool for the detection of potential residual tumor foci.

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Aygül Mert, Barbara Kiesel, Adelheid Wöhrer, Mauricio Martínez-Moreno, Georgi Minchev, Julia Furtner, Engelbert Knosp, Stefan Wolfsberger and Georg Widhalm

OBJECT

Surgery of suspected low-grade gliomas (LGGs) poses a special challenge for neurosurgeons due to their diffusely infiltrative growth and histopathological heterogeneity. Consequently, neuronavigation with multimodality imaging data, such as structural and metabolic data, fiber tracking, and 3D brain visualization, has been proposed to optimize surgery. However, currently no standardized protocol has been established for multimodality imaging data in modern glioma surgery. The aim of this study was therefore to define a specific protocol for multimodality imaging and navigation for suspected LGG.

METHODS

Fifty-one patients who underwent surgery for a diffusely infiltrating glioma with nonsignificant contrast enhancement on MRI and available multimodality imaging data were included. In the first 40 patients with glioma, the authors retrospectively reviewed the imaging data, including structural MRI (contrast-enhanced T1-weighted, T2-weighted, and FLAIR sequences), metabolic images derived from PET, or MR spectroscopy chemical shift imaging, fiber tracking, and 3D brain surface/vessel visualization, to define standardized image settings and specific indications for each imaging modality. The feasibility and surgical relevance of this new protocol was subsequently prospectively investigated during surgery with the assistance of an advanced electromagnetic navigation system in the remaining 11 patients. Furthermore, specific surgical outcome parameters, including the extent of resection, histological analysis of the metabolic hotspot, presence of a new postoperative neurological deficit, and intraoperative accuracy of 3D brain visualization models, were assessed in each of these patients.

RESULTS

After reviewing these first 40 cases of glioma, the authors defined a specific protocol with standardized image settings and specific indications that allows for optimal and simultaneous visualization of structural and metabolic data, fiber tracking, and 3D brain visualization. This new protocol was feasible and was estimated to be surgically relevant during navigation-guided surgery in all 11 patients. According to the authors' predefined surgical outcome parameters, they observed a complete resection in all resectable gliomas (n = 5) by using contour visualization with T2-weighted or FLAIR images. Additionally, tumor tissue derived from the metabolic hotspot showed the presence of malignant tissue in all WHO Grade III or IV gliomas (n = 5). Moreover, no permanent postoperative neurological deficits occurred in any of these patients, and fiber tracking and/or intraoperative monitoring were applied during surgery in the vast majority of cases (n = 10). Furthermore, the authors found a significant intraoperative topographical correlation of 3D brain surface and vessel models with gyral anatomy and superficial vessels. Finally, real-time navigation with multimodality imaging data using the advanced electromagnetic navigation system was found to be useful for precise guidance to surgical targets, such as the tumor margin or the metabolic hotspot.

CONCLUSIONS

In this study, the authors defined a specific protocol for multimodality imaging data in suspected LGGs, and they propose the application of this new protocol for advanced navigation-guided procedures optimally in conjunction with continuous electromagnetic instrument tracking to optimize glioma surgery.

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Matthias Millesi, Barbara Kiesel, Mario Mischkulnig, Mauricio Martínez-Moreno, Adelheid Wöhrer, Stefan Wolfsberger, Engelbert Knosp and Georg Widhalm

OBJECTIVE

One of the most important causes for recurrence of intracranial meningiomas is residual tumor tissue that remains despite assumed complete resection. Recently, intraoperative visualization of meningioma tissue by 5-aminolevulinic acid (5-ALA)–induced protoporphyrin IX (PpIX) fluorescence was reported. The aim of this study was to investigate the possible surgical benefits of PpIX fluorescence for detection of meningioma tissue.

METHODS

5-ALA was administered preoperatively to 190 patients undergoing resection of 204 intracranial meningiomas. The meningiomas' PpIX fluorescence status, fluorescence quality (strong or vague), and intratumoral fluorescence homogeneity were investigated during surgery. Additionally, specific sites, including the dural tail, tumor-infiltrated bone flap, adjacent cortex, and potential satellite lesions, were analyzed for PpIX fluorescence in selected cases.

RESULTS

PpIX fluorescence was observed in 185 (91%) of 204 meningiomas. In the subgroup of sphenoorbital meningiomas (12 of 204 cases), the dural part showed visible PpIX fluorescence in 9 cases (75%), whereas the bony part did not show any PpIX fluorescence in 10 cases (83%). Of all fluorescing meningiomas, 168 (91%) showed strong PpIX fluorescence. Typically, most meningiomas demonstrated homogeneous fluorescence (75% of cases). No PpIX fluorescence was observed in any of the investigated 89 dural tails. In contrast, satellite lesions could be identified through PpIX fluorescence in 7 cases. Furthermore, tumor-infiltrated bone flaps could be visualized by PpIX fluorescence in all 13 cases. Notably, PpIX fluorescence was also present in the adjacent cortex in 20 (25%) of 80 analyzed cases.

CONCLUSIONS

The authors' data from this largest patient cohort to date indicate that PpIX fluorescence enables intraoperatively visualization of most intracranial meningiomas and allows identification of residual tumor tissue at specific sites. Thus, intraoperative detection of residual meningioma tissue by PpIX fluorescence might in future reduce the risk of recurrence.

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Christian Dorfer, Georgi Minchev, Thomas Czech, Harald Stefanits, Martha Feucht, Ekaterina Pataraia, Christoph Baumgartner, Gernot Kronreif and Stefan Wolfsberger

OBJECTIVE

The authors' group recently published a novel technique for a navigation-guided frameless stereotactic approach for the placement of depth electrodes in epilepsy patients. To improve the accuracy of the trajectory and enhance the procedural workflow, the authors implemented the iSys1 miniature robotic device in the present study into this routine.

METHODS

As a first step, a preclinical phantom study was performed using a human skull model, and the accuracy and timing between 5 electrodes implanted with the manual technique and 5 with the aid of the robot were compared. After this phantom study showed an increased accuracy with robot-assisted electrode placement and confirmed the robot's ability to maintain stability despite the rotational forces and the leverage effect from drilling and screwing, patients were enrolled and analyzed for robot-assisted depth electrode placement at the authors' institution from January 2014 to December 2015. All procedures were performed with the S7 Surgical Navigation System with Synergy Cranial software and the iSys1 miniature robotic device.

RESULTS

Ninety-three electrodes were implanted in 16 patients (median age 33 years, range 3–55 years; 9 females, 7 males). The authors saw a significant increase in accuracy compared with their manual technique, with a median deviation from the planned entry and target points of 1.3 mm (range 0.1–3.4 mm) and 1.5 mm (range 0.3–6.7 mm), respectively. For the last 5 patients (31 electrodes) of this series the authors modified their technique in placing a guide for implantation of depth electrodes (GIDE) on the bone and saw a significant further increase in the accuracy at the entry point to 1.18 ± 0.5 mm (mean ± SD) compared with 1.54 ± 0.8 mm for the first 11 patients (p = 0.021). The median length of the trajectories was 45.4 mm (range 19–102.6 mm). The mean duration of depth electrode placement from the start of trajectory alignment to fixation of the electrode was 15.7 minutes (range 8.5–26.6 minutes), which was significantly faster than with the manual technique. In 12 patients, depth electrode placement was combined with subdural electrode placement. The procedure was well tolerated in all patients. The authors did not encounter any case of hemorrhage or neurological deficit related to the electrode placement. In 1 patient with a psoriasis vulgaris, a superficial wound infection was encountered. Adequate physiological recordings were obtained from all electrodes. No additional electrodes had to be implanted because of misplacement.

CONCLUSIONS

The iSys1 robotic device is a versatile and easy to use tool for frameless implantation of depth electrodes for the treatment of epilepsy. It increased the accuracy of the authors' manual technique by 60% at the entry point and over 30% at the target. It further enhanced and expedited the authors' procedural workflow.

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Barbara Kiesel, Matthias Millesi, Adelheid Woehrer, Julia Furtner, Anahita Bavand, Thomas Roetzer, Mario Mischkulnig, Stefan Wolfsberger, Matthias Preusser, Engelbert Knosp and Georg Widhalm

OBJECTIVE

Stereotactic needle biopsies are usually performed for histopathological confirmation of intracranial lymphomas to guide adequate treatment. During biopsy, intraoperative histopathology is an effective tool to avoid acquisition of nondiagnostic samples. In the last years, 5-aminolevulinic acid (5-ALA)–induced fluorescence has been increasingly used for visualization of diagnostic brain tumor tissue during stereotactic biopsies. Recently, visible fluorescence was reported in the first cases of intracranial lymphomas as well. The aim of this study is thus to investigate the technical and clinical utility of 5-ALA–induced fluorescence in a large series of stereotactic biopsies for intracranial lymphoma.

METHODS

This prospective study recruited adult patients who underwent frameless stereotactic needle biopsy for a radiologically suspected intracranial lymphoma after oral 5-ALA administration. During biopsy, samples from the tumor region were collected for histopathological analysis, and presence of fluorescence (strong, vague, or no fluorescence) was assessed with a modified neurosurgical microscope. In tumors with available biopsy samples from at least 2 different regions the intratumoral fluorescence homogeneity was additionally investigated. Furthermore, the influence of potential preoperative corticosteroid treatment or immunosuppression on fluorescence was analyzed. Histopathological tumor diagnosis was established and all collected biopsy samples were screened for diagnostic lymphoma tissue.

RESULTS

The final study cohort included 41 patients with intracranial lymphoma. Stereotactic biopsies with assistance of 5-ALA were technically feasible in all cases. Strong fluorescence was found as maximum level in 30 patients (75%), vague fluorescence in 2 patients (4%), and no visible fluorescence in 9 patients (21%). In 28 cases, samples were obtained from at least 2 different tumor regions; homogenous intratumoral fluorescence was found in 16 of those cases (57%) and inhomogeneous intratumoral fluorescence in 12 (43%). According to histopathological analysis, all samples with strong or vague fluorescence contained diagnostic lymphoma tissue, resulting in a positive predictive value of 100%. Analysis showed no influence of preoperative corticosteroids or immunosuppression on fluorescence.

CONCLUSIONS

The data obtained in this study demonstrate the technical and clinical utility of 5-ALA–induced fluorescence in stereotactic biopsies of intracranial lymphomas. Thus, 5-ALA can serve as a useful tool to select patients not requiring intraoperative histopathology, and its application should markedly reduce operation time and related costs in the future.