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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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Ayguel Wurzer, Georgi Minchev, Claudia Cervera-Martinez, Alexander Micko, Gernot Kronreif, and Stefan Wolfsberger

OBJECTIVE

Electromagnetic (EM) navigation provides the advantages of continuous guidance and tip-tracking of instruments. The current solutions for patient reference trackers are suboptimal, as they are either invasively screwed to the bone or less accurate if attached to the skin. The authors present a novel EM reference method with the tracker rigidly but not invasively positioned inside the nasal cavity.

METHODS

The nasal tracker (NT) consists of the EM coil array of the AxiEM tracker plugged into a nasal tamponade, which is then inserted into the inferior nasal meatus. Initially, a proof-of-concept study was performed on two cadaveric skull bases. The stability of the NT was assessed in simulated surgical situations, for example, prone, supine, and lateral patient positioning and skin traction. A deviation ≤ 2 mm was judged sufficiently accurate for clinical trial. Thus, a feasibility study was performed in the clinical setting. Positional changes of the NT and a standard skin-adhesive tracker (ST) relative to a ground-truth reference tracker were recorded throughout routine surgical procedures. The accuracy of the NT and ST was compared at different stages of surgery.

RESULTS

Ex vivo, the NT proved to be highly stable in all simulated surgical situations (median deviation 0.4 mm, range 0.0–2.0 mm). In 13 routine clinical cases, the NT was significantly more stable than the ST (median deviation at procedure end 1.3 mm, range 0.5–3.0 mm vs 4.0 mm, range 1.2–11.2 mm, p = 0.002). The loss of accuracy of the ST was highest during draping and flap fixation.

CONCLUSIONS

Application of the EM endonasal patient tracker was found to be feasible with high procedural stability ex vivo as well as in the clinical setting. This innovation combines the advantages of high precision and noninvasiveness and may, in the future, enhance EM navigation for neurosurgery.

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Georgi Minchev, Ayguel Wurzer, Wolfgang Ptacek, Gernot Kronreif, Alexander Micko, Christian Dorfer, and Stefan Wolfsberger

OBJECTIVE

Consistently high accuracy and a straightforward use of stereotactic guidance systems are crucial for precise stereotactic targeting and a short procedural duration. Although robotic guidance systems are widely used, currently available systems do not fully meet the requirements for a stereotactic guidance system that combines the advantages of frameless surgery and robotic technology. The authors developed and optimized a small-scale yet highly accurate guidance system that can be seamlessly integrated into an existing operating room (OR) setup due to its design. The aim of this clinical study is to outline the development of this miniature robotic guidance system and present the authors’ clinical experience.

METHODS

After extensive preclinical testing of the robotic stereotactic guidance system, adaptations were implemented for robot fixation, software usability, navigation integration, and end-effector application. Development of the robotic system was then advanced in a clinical series of 150 patients between 2013 and 2019, including 111 needle biopsies, 13 catheter placements, and 26 stereoelectroencephalography (SEEG) electrode placements. During the clinical trial, constant modifications were implemented to meet the setup requirements, technical specifications, and workflow for each indication. For each application, specific setup, workflow, and median procedural accuracy were evaluated.

RESULTS

Application of the miniature robotic system was feasible in 149 of 150 cases. The setup in each procedure was successfully implemented without adding significant OR time. The workflow was seamlessly integrated into the preexisting procedure. In the course of the study, procedural accuracy was improved. For the biopsy procedure, the real target error (RTE) was reduced from a mean of 1.8 ± 1.03 mm to 1.6 ± 0.82 mm at entry (p = 0.05), and from 1.7 ± 1.12 mm to 1.6 ± 0.72 mm at target (p = 0.04). For the SEEG procedures, the RTE was reduced from a mean of 1.43 ± 0.78 mm in the first half of the procedures to 1.12 ± 0.52 mm (p = 0.002) at entry in the second half, and from 1.82 ± 1.13 mm to 1.57 ± 0.98 mm (p = 0.069) at target, respectively. No healing complications or infections were observed in any case.

CONCLUSIONS

The miniature robotic guidance device was able to prove its versatility and seamless integration into preexisting workflow by successful application in 149 stereotactic procedures. According to these data, the robot could significantly improve accuracy without adding time expenditure.

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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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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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Alice Senta Ryba, Juan Sales-Llopis, Stefan Wolfsberger, Aki Laakso, Roy Thomas Daniel, and Pablo González-López

Hemangioblastomas (HBs) are rare, benign, hypervascularized tumors. Fluorescent imaging with indocyanine green (ICG) can visualize tumor angioarchitecture. The authors report a case of multiple HBs involving two radiologically silent lesions only detected intraoperatively by ICG fluorescence. A 26-year-old woman presented with a cystic cerebellar mass on the tentorial surface of the left cerebellar hemisphere on MRI. A left paramedian suboccipital approach was performed to remove the mural nodule with the aid of ICG injection. The first injection, applied just prior to removing the nodule, highlighted the tumor and vessels. After resection, two new lesions, invisible on the preoperative MRI, surprisingly enhanced on fluorescent imaging 35 minutes after the ICG bolus. Both silent lesions were removed. Histological analysis of all three lesions revealed they were positive for HB. The main goal of this report is to hypothesize possible explanations about the mechanism that led to the behavior of the two silent lesions. Intraoperative ICG videoangiography was useful to understand the 3D angioarchitecture and HB flow patterns to perform a safe and complete resection in this case. Understanding the HB ultrastructure and pathophysiological mechanisms, in conjunction with the properties of ICG, may expand potential applications for their diagnosis and future treatments.

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Alexander Micko, Arthur Hosmann, Aygül Wurzer, Svenja Maschke, Wolfgang Marik, Engelbert Knosp, and Stefan Wolfsberger

OBJECTIVE

The transsphenoidal route to pituitary adenomas challenges surgeons because of the highly variable sinunasal anatomy. Orientation may be improved if the appropriate information is provided intraoperatively by image guidance. The authors developed an advanced image guidance protocol dedicated to sinunasal surgery that extracts information from multiple modalities and forms it into a single image that includes fine sinunasal structures and arteries.

The aim of this study was to compare the advantages of this novel image guidance protocol with the authors’ previous series, with emphasis on anatomical structures visualized and complication rate.

METHODS

This retrospective analysis comprised 200 patients who underwent surgery for pituitary adenoma via a transnasal transsphenoidal endoscopic approach. The authors’ standard image guidance protocol consisting of CT for solid bone, T1CEMRI for soft tissues, and MRA for the carotid artery was applied in 100 consecutive cases. The advanced image guidance protocol added a first-hit ray casting of the CT scan for visualization of fine sinunasal structures, and adjustments to the MRA to visualize the sphenopalatine artery (SPA) were applied in a subsequent 100 consecutive cases.

RESULTS

A patent sphenoid ostium—i.e., an ostium not covered by a mucosal layer—was visualized significantly more often by the advanced protocol than the standard protocol (89% vs 40%, p < 0.001) in primary surgeries. The SPA and its branches were only visualized by the advanced protocol (87% and 91% of cases in primary surgeries and reoperations, respectively) and not once by the standard protocol. The number of visualized complete and incomplete sphenoid septations matched significantly more commonly with the surgical view when using the advanced protocol than the standard protocol at primary operation (mean 1.9 vs 1.6, p < 0.001). However, in 25% of all cases a complex and not a simple sinus anatomy was present. In comparison with the intraoperative results, a complex sphenoid sinus anatomy was always detected by the advanced but not by the standard protocol (25% vs 8.5%, p = 0.001).

Furthermore, application of the advanced protocol reduced the cumulative rate of complications (25% vs 18% [standard vs advanced group]). Although an overall significant difference could not be determined (p = 0.228), a subgroup analysis of reoperations (35/200) revealed a significantly lower rate of complications in the advanced group (5% vs 30%, p = 0.028).

CONCLUSIONS

The data show that the advanced image guidance protocol could intraoperatively visualize the fine sinunasal sinus structures and small arteries with a high degree of detail. By improving intraoperative orientation, this may help to reduce the rate of complications in endoscopic transsphenoidal surgery, especially in reoperations.

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Alexander Micko, Johannes Oberndorfer, Wolfgang J. Weninger, Greisa Vila, Romana Höftberger, Stefan Wolfsberger, and Engelbert Knosp

OBJECTIVE

Parasellar growth is one of the most important prognostic variables of pituitary adenoma surgery, with adenomas regarded as not completely resectable if they invade the cavernous sinus (CS) but potentially curable if they displace CS structures. This study was conducted to correlate surgical treatment options and outcomes to the different biological behaviors (invasion vs displacement) of adenomas with parasellar extension into the superior or inferior CS compartments or completely encasing the carotid artery (Knosp high grades 3A, 3B, and 4).

METHODS

This was a retrospective cohort analysis of 106 consecutive patients with Knosp high-grade pituitary adenomas with parasellar extension who underwent surgery via a primary endoscopic transsphenoidal approach between 2003 and 2017. Biological tumor characteristics (surgical status of invasiveness and tumor texture, 2017 WHO classification, proliferation rate), extent of resection, and complication rate were correlated with parasellar extension grades 3A, 3B, and 4 on preoperative MRI studies.

RESULTS

Invasiveness was significantly less common in grade 3A (44%) than in grade 3B (72%, p = 0.037) and grade 4 (100%, p < 0.001) adenomas. Fibrous tumor texture was significantly more common in grade 4 (52%) compared to grade 3A (20%, p = 0.002), but not compared to grade 3B (28%) adenomas. Functioning macroadenomas had a significantly higher rate of invasiveness than nonfunctioning adenomas (91% vs 55%, p = 0.002). Mean proliferation rate assessed by MIB-1 was > 3% in all groups but without significant difference between the groups (grade 3A, 3.2%; 3B, 3.9%; 4, 3.7%). Rates of endocrine remission/gross-total resection were significantly higher in grade 3A (64%) than in grade 3B (33%, p = 0.021) and grade 4 (0%, p < 0.001) adenomas. In terms of complication rates, no significant difference was observed between grades.

CONCLUSIONS

According to the authors’ data, the biological behavior of pituitary adenomas varies significantly between parasellar extension patterns. Adenomas with extension into the superior CS compartment have a lower rate of invasive growth than adenomas extending into the inferior CS compartment or encasing the carotid artery. Consequently, a significantly higher rate of remission can be achieved in grade 3A than in grade 3B and grade 4 adenomas. Therefore, the distinction into grades 3A, 3B, and 4 is of importance for prediction of adenoma invasion and surgical treatment considerations.

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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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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.