An Advanced Navigation Protocol for Endoscopic Transsphenoidal Surgery

Peer-Review Reports

An Advanced Navigation Protocol for Endoscopic Transsphenoidal Surgery Ayguel Mert1, Alexander Micko1, Markus Donat1, Manuela Maringer1, Katja Buehler 2, Garnette R. Sutherland 3, Engelbert Knosp1, Stefan Wolfsberger, MD1,3

Key words Accuracy - Endoscopy - Multimodality navigation - Transsphenoidal pituitary surgery -

Abbreviations and Acronyms CT: Computed tomography EM: Electromagnetic ICA: Internal carotid artery MR: Magnetic resonance From the 1Department of Neurosurgery, Medical University Vienna, Austria; 2VRVis Research Centre for Virtual Reality and Visualization GmbH, Vienna, Austria; and 3Department of Clinical Neurosciences, Division of Neurosurgery, University of Calgary, Canada To whom correspondence should be addressed: Stefan Wolfsberger, M.D. [E-mail: [email protected]] Citation: World Neurosurg. (2014) 82, 6S:S95-S105. http://dx.doi.org/10.1016/j.wneu.2014.07.032 Journal homepage: www.WORLDNEUROSURGERY.org Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2014 Published by Elsevier Inc.

INTRODUCTION Whereas the conventional transsphenoidal approach to sellar lesions is strictly confined to the midline by means of the nasal speculum and the linear optical axis of the operating microscope (21), the extended lateral field-of-view and maneuverability of the endoscopic technique implies a loss of this strict midline orientation (4, 25). Although this is an advantage for resecting parasellar tumor extensions, it raises the danger of injury to the internal carotid artery (ICA) that, along with meningitis, accounts for most of the low percentage of mortality (0.2%e0.9% in large series) of transsphenoidal pituitary surgery (6, 8, 13, 15, 31). For intraoperative guidance, Guiot and Thibaut (19) introduced fluoroscopy to transsphenoidal surgery in the late fifties; however, plain radiograph views limited to the sagittal plane do not provide critical information concerning laterality. Therefore, neuronavigation systems, which by

- OBJECTIVE:

To report our clinical experience with an advanced navigation protocol that provides seamless integration into the operating workflow of endoscopic transsphenoidal surgery.

- PATIENTS

AND METHODS: From 32 consecutive cases of endoscopic transsphenoidal surgery, an optimal setup of continuous electromagnetic instrument navigation was created. Additionally, our standard multimodality image navigation of T1-weighted magnetic resonance (MR) images for soft tissue, MR angiogram for vascular structures, and computed tomography (CT) for solid bone was advanced by the addition of a CT surface rendering for fine paranasal sinus structures. The anatomic structures visualized and their clinical impacts were compared between standard and advanced visualization protocol. Bone-windowed CT images served as reference. The accuracy of the navigation setup was assessed by intraoperative landmark tests. Potential tissue shift was calculated by comparing pre- and postoperative MR angiograms of 20 macroadenomas.

- RESULTS:

After a learning curve of 2 cases (1 ferromagnetic interference and 1 dislocation of the patient reference tracker), the advanced navigation protocol was feasible in 30 cases. Advanced multimodality imaging was able to visualize significantly finer paranasal sinus structures than multimodality image navigation without CT surface rendering, equal to bone-windowed CT images (P < 0.001, McNemar test). This was found helpful for orientation in cases of complex sphenoid sinus anatomy. The accuracy of the advanced navigation setup corresponded to standard optic navigation with skull fixation. A tissue shift of median 2 mm (range 0e9 mm) was observed in the posterior genu of the internal carotid arteries after tumor resection.

- CONCLUSIONS:

The advanced navigation protocol permits continuous suction-tracked navigation guidance during endoscopic transsphenoidal surgery and optimal visualization of solid bone, fine paranasal sinus structures, softtissue and vascular structures. This may add to the safety of the procedure especially in cases of anatomical variations and in cases of recurrent adenomas with distorted anatomy.

reconstruction of image data provide the surgeon with multiplanar views, have found wide acceptance for use in endoscopic transsphenoidal surgery (5, 11, 12, 16, 26, 27, 30, 34, 35, 38, 40, 50, 55). Additionally, navigation systems offer the possibility to combine multiple imaging modalities, each optimized for specific anatomic structures that are necessary to visualize during the different stages of the procedure, to one single “multimodality” image. Until recently, our protocol of multimodality visualization for standard

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navigation included magnetic resonance (MR) for pituitary and vascular anatomy and computed tomography (CT) for solid bone structures (35). Fine paranasal sinus structures such as mucosa, ethmoid air cells, sphenoid ostia, and sphenoid septations, however, that are necessary to comprehend for an optimal exposure of the surgical target, remained largely invisible on the navigation image. Furthermore, our previous navigation setup was based on optic tracking technology, whereby the endoscope commonly

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blocked the line-of-sight between navigation probe and camera bar. Advanced electromagnetic (EM) tracking technology has completely overcome this line-of-sight issue and can provide continuous suction tip tracking during endoscopic transsphenoidal surgery. Furthermore, a firmly affixed adhesive patient tracker on the patient’s forehead may obviate the need for rigid head fixation in a skull clamp, provide head mobility during surgery, and add to patient comfort postoperatively (47). Navigation systems are based on preoperative radiological image data, and tissue-shift after tumor resection is a wellknown cause of diminished accuracy during intracranial surgery (45). At later stages of transsphenoidal adenoma resection, medial shifting of the ICA is therefore not updated by the system and may pose a potential hazard if unexpected by the surgeon. The aim of this study was to report our clinical experience with an advanced navigation protocol for endoscopic transsphenoidal surgery that for the first time adds precise display of fine paranasal sinus structures to the multimodality visualization of the surgical anatomy and provides a seamless integration into the operating workflow by continuous EM suction navigation. Further, we evaluated the accuracy of neuronavigation during this procedure and determined whether there was shifting of the ICA after tumor resection. PATIENTS AND METHODS Since 2002, a total of 268 endoscopic transsphenoidal surgeries have been performed with navigation guidance at the Department of Neurosurgery of the Medical University Vienna. For details of our standard navigation protocol until 2011, see Table 1 and McGrath et al. (35). Following the introduction of a latest generation navigation system (StealthStation S7, Medtronic, Colorado, USA) in September 2011, we advanced our navigation protocol with continuous EM instrument navigation and with additional display of fine paranasal sinus structures in the multimodality visualization. This work describes our setup of and clinical experience with an advanced navigation protocol for endoscopic transsphenoidal surgery, its clinical value,

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ADVANCED NAVIGATION PROTOCOL FOR ENDOSCOPIC TRANSSPHENOIDAL SURGERY

Table 1. Navigation System Setup Navigation Technique Standard

Advanced

Time period

2002e2011

2011e2012

No. patients

268

32

Medtronic Treon, S7 (Cranial 2.1)

Medtronic S7 (Cranial 2.2)

Optic

Electromagnetic

Navigation system/software version Tracking technique Registration

Hybrid

Surface-based

Yes (skull clamp)

No (horseshoe)

Skull clamp via arm

Forehead

Instrument tracking

Suction

Suction

Position of tracking

Handle

Tip

Suretrack (frame with spheres)

EM stylet (wire with coils)

Soft tissue (MR T1 CE)

þ

þ

Arteries (MRA)

þ

þ

Solid bone (CT)

þ

þ

N/A

þ

Rigid head fixation necessary Patient reference tracker position

System Multimodality visualization

Fine paranasal sinus structures (CT)

MR, magnetic resonance; CE, contrast enhanced; MRA, magnetic resonance angiography; CT, computed tomograpy.

benefits over standard navigation, and accuracy. Image Data Computed Tomography. Assessment of bony nasal and sphenoid anatomy by CT is part of our routine preoperative diagnostic workup in patients with pituitary adenoma. A cranial CT scan was acquired on a Siemens Somatom Sensation 64 CT scanner (Siemens Medical Systems, Erlangen, Germany) starting inferior to the nares and advancing at a 1-mm spiral distance with 0 degrees gantry tilt, a fixed tube voltage of 120 kV, and a current of 380 mA. MR Tomography. All image data were acquired on a 3.0T MR system (Siemens Magnetom Trio). For visualization of softtissue structures a T1-weighted. contrastenhanced 3-dimensional gradient echo sequence (acquisition time 5.34 minutes, repetition time 1800 milliseconds, echo time 3.79 milliseconds, 256 matrix, field of view 220 mm, flip angle 12
, slice thickness 1 mm, 192 slices) was obtained. For visualization of vascular anatomy we used 3-dimensional time-of-flight MR angiogram (acquisition time 4.42 minutes, repetition time

22 milliseconds, echo time 3.86 milliseconds, 512 matrix, field of view 200 mm, slice thickness 0.65 mm, 100 slices). Advanced Navigation Setup Multimodality Visualization. Initially, 4 radiographic image stacks (2 identical CT, T1-weighted, contrast-enhanced MR, MR angiogram) were transferred from the hospital picture archiving and communication system into the navigation system via the local network. Because of its superior registration accuracy compared with MR, the CT images were used as reference data for image fusion and patient registration. Image data were automatically merged using the manufacturer’s image fusion module. The concurrent visualization of selective anatomy from the 4 imaging modalities was achieved by applying the system settings outlined in Table 2. Thereby, a specific colormap and windowing, which control color and opacity of each voxel intensity, are assigned to each imaging modality. For display of soft-tissue structures such as pituitary adenoma and gland, cavernous sinus structures, optic nerves, and chiasm,

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Table 2. Multimodality Imaging Setup System Settings Imaging Modality

For Visualization of.

Colormap

Level

Width

MR T1 CE

Soft tissue (adenoma, pituitary gland, cavernous sinus)

Grayscale

System preset

System preset

CT

Solid bone

Bone

Min w/o background noise

Max

CT

Fine paranasal sinus structures (sphenoid sinus septations)

Bone

480  140

700  180

MRA (TOF)

ICA, ACA, ophtA

Vessels

Min w/o background noise

Max

MR, magnetic resonance; CE, contrast enhanced; CT, computed tomography; MRA, magnetic resonance angiography; TOF, time of flight, ICA, interanal cartoid artery; anterior cerebral artery; ophtA, ophthalmic artery.

T1-weighted, contrast-enhanced MR was rendered in a standard grayscale colormap (Figure 1A). Vascular anatomy such as the ICA was derived from MR angiogram in “vessel” colormap (35). Solid bone, such as nasal septum, sphenoid sinus rostrum, or dorsum sellae, was derived from 1 of 2 identical CT image stacks by applying the standard “bone” colormap. Thereby, all remaining tissue apart from bone was displayed transparent (Figure 1B). For the advanced navigation protocol, we developed the possibility of displaying fine paranasal sinus structures (such as sphenoid ostia, sphenoid sinus septations, ethmoid air cells) from the second CT image stack, which was displayed in “bone” colormap with window settings that resulted in a thinlined surface rendering at the air / tissue border (Figure 1C). Surgical Planning. For surgical planning, we checked for potential anatomic variations along a trajectory from a nostril to the tumor and adjusted our surgical plan accordingly (e.g., ipsi- or contralateral approach to the maximum parasellar extension of the adenoma, removal of middle turbinate). EM Navigation System Setup. Our surgeon’s position was behind the patient’s head. The head was placed in a horseshoe headrest or alternatively rigidly fixed in a nonferromagnetic skull clamp (Figure 2A). The optimum EM field emitter position was found in line with and approximately 15 cm lateral to the left ear. This allowed lefthanded suction tracking uninterrupted from the metal of the endoscope. The self-adhesive patient reference tracker was fixed on the median forehead or on the skull clamp at approximately 25 cm distance from the

emitter. Patient-to-image registration was performed with a surface-based algorithm that collects 350 points from a probe’s movements over the patient’s skin. Registration accuracy was always checked on 6 anatomic landmarks (nasion, philtrum, 2 canthus, 2 tragus). For continuous instrument navigation, we used the “stylet,” which is a flexible wire originally designed for shunt catheter placement with 2 EM field detecting coils close to its tip, and inserted this probe into a 3-mm diameter standard suction tube (Figure 2B) (22). Evaluation Feasibility. Clinical experience was used to improve the advanced navigation setup to the final protocol as described previously. For reproducibility, we tested the CT surface rendering on navigation data from scanners of other manufacturers. Clinical Value. To assess the advantages of the advanced multimodality visualization over our previous setup, we compared the anatomic structures visualized in advanced navigation versus standard navigation in 40 consecutive cases of pituitary macroadenoma (20 from our standard navigation series and 20 from the advanced navigation series). Bone-windowed CT images served as the reference for visualization of fine paranasal sinus structures. Further, we evaluated the surgical value of each structure visualized (see Table 3). Accuracy. Intraoperative accuracy was checked in both groups with repeated landmark tests on bony sphenoid sinus landmarks (craniocaudal septations for horizontal inaccuracy and indentations of clivus and tuberculum sellae for vertical

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inaccuracy, see Figure 3) using the suction tube. Navigation was abandoned if judged inaccurate at this stage. Tissue Shift. A potential medial shifting of the ICA after tumor resection was evaluated in the 20 patients of the standard navigation group as a measure for the continuing accuracy of the system. Therefore, we performed a second MR angiogram postoperatively either during the same hospital stay or at early follow-up. By means of the navigation system software, the postoperative MR angiogram was fused onto the preoperative MR angiogram images and color-coded for easy distinguishability. Then, the distances between the ICAs of either side were calculated at well-defined points (posterior genu, sagittal part, anterior genu, supraclinoid ICA, Figure 4). Subtraction of pre- and postoperative ICA distances rendered the tissue shift. This shift was then correlated with: 1) tumor volume, to assess a potential relation between tissue shift and tumor size; and 2) the time interval between surgery and postoperative MR angiogram, to rule out time-dependency of shifting.

Statistical Analysis For statistical analyses SPSS version 19.0 software (SPSS Inc., Chicago, Illinois, USA) was used. Sensitivity and specificity of the advanced navigation and standard navigation versus bone window CT to display fine paranasal sinus structure were calculated using McNemar test. Correlation was performed using Pearson’s coefficient. A P < 0.05 was considered significant. Measurements are expressed as median and range values.

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Figure 1. Multimodality visualization of nonfunctioning macroadenoma: (A) T1-weighted contrast-enhanced magnetic resonance imaging (MRI) does not visualize the bony sphenoid sinus anatomy sufficiently. (B) Standard multimodality image fusion (T1-weighted, contrast-enhanced, MR angiogram, computed tomography [CT]) visualizes soft tissue and vascular and solid bony anatomy in the area of the cavernous sinus. (C) The

RESULTS The proposed advanced navigation protocol was applied in 32 cases of endoscopic transsphenoidal surgery.

Feasibility EM Navigation. During the initial month of application, a learning curve was encountered for the EM navigation system

Figure 2. Operating room setup. (A) The surgeon’s position is behind the head of the patient, who is placed in a horseshoe headrest. The optimum EM field emitter (E) position is in line with and approximately 15 cm lateral to the left ear. The self-adhesive patient reference tracker (T) is fixed on the median forehead at approximately 25 cm distance from the emitter and

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advanced navigation protocol adds surface-rendering from the identical CT scan to concurrently display fine paranasal sinus anatomy thereby improving orientation during the approach. Note the complete septum on the right side (C), an incomplete septum on the left (i) and the posterior ethmoid air cells (E).

setup. The application of the patient reference tracker close to a standard ferromagnetic skull clamp caused persistent EM field reception failure during

taped to the headrest to prevent inadvertent movement. (B) For continuous instrument navigation, the EM stylet, a flexible wire with 2 electromagnetic field detecting coils at its tip (red bars), is introduced into a standard single-use suction.

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Table 3. Multimodality Visualization Multimodality Navigation Advanced Stage of Approach/Anatomical Structure (n [ 40 Patients)

n

(%)

Standard n

CT Bone Windowed

(%)

n

(%)

Clinical Impact

Nasal stage Septal deviation

17

(43%)

17

(43%)

17

(43%)

Septal spur

22

(55%)

22

(55%)

22

(55%)

Sphenoid ostium visible (80 sides)

68

(85%)

26

(33%)

68

(85%)

Choice of side of approach

Direction of approach

Sphenoid stage* Complete sphenoid septations No. of complete septations/pat, median (range) Incomplete sphenoid septations No. of incomplete septations/patient median (range)

52

31

53

1 (0e3)

1 (0e2)

1 (0e3)

25

30

25

0 (0e3)

1 (0e3)

0 (0e3)

Median septum deviated

18

(46%)

16

(41%)

Septum inserting at ICA protruberance

13

(33%)

8

Horizontal septum

12

(31%)

5

Onodi cell Sellar floor (partially) eroded

17

(44%)

(21%)

4

(10%)

(13%)

12

(31%)

3

(8%)

0

(0%)

3

(8%)

21

(53%)

21

(53%)

21

(53%)

Orientation inside sphenoid sinus, removal of septations

Drilling required?

Sellar stage Distance of ICA at sellar floor (median/range)

20 mm (12e32)

e

Safe opening of sellar floor

Tumor extension lateral to medial ICA border, median (range)

3 mm (0e16)

e

Tumor resection

Dorsum sellae (partially) arroded

14

(35%)

14

(35%)

14

(35%)

CT, computed tomography; ICA, internal carotid artery. *No data in one patient with conchal type sinus.

surgery in one patient. Thereafter, rigid head fixation was abandoned, and the patient was positioned in a horseshoe with the reference tracker attached to the forehead (47). Inadvertent tension on the patient draping caused transient movement of the patient galea and consecutive shift of the skin-attached reference tracker resulting in sudden inaccuracy of the system in another case. After we fixed the reference tracker via tape to the horseshoe, this failure has not reoccurred. Rigid fixation of the patient head in a nonferromagnetic skull clamp is another possible solution. Apart from this initial learning curve, the advanced navigation setup was technically feasible in 30 cases, as outlined in the protocol of the section Patients and Methods.

Multimodality Visualization. Multimodality visualization was feasible in all cases. We tested the CT surface rendering for display of fine paranasal sinus structures on image data derived from scanners by other manufacturers (e.g., Siemens, Philips, GE) with success. However, threshold settings vary and need to be adapted for each scanner model and sequence. Table 2 provides the results applicable on our own aforementioned scanner for reference. Anatomical Structures Visualized and Their Clinical Value Standard and advanced multimodality visualization protocols were equal in depicting solid bone anatomy. Because of the addition of surface rendering CT, the advanced was superior to the standard protocol for display

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of fine paranasal sinus structures: Sphenoid sinus septations were significantly more often completely displayed with advanced than with standard navigation (P < 0.001, McNemar test). Furthermore, the advanced protocol was able to depict the position of the sphenoid ostium more precisely than standard navigation, which usually showed a large communication between nasal cavity and sphenoid sinus (P < 0.001, McNemar test). Overall, the advanced visualization protocol was equal to bone-window CT in terms of visualization of fine paranasal sinus structures (Table 3). During the nasal stage of the procedure, the solid bone CT component of the navigation image was of value for choosing the side of approach by visualizing bony nasal structures and its variations. Using

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Figure 3. Intraoperative accuracy check: landmark tests need to be repeatedly performed on bony sphenoid sinus landmarks during surgery. (A) Suction tube on craniocaudal midline septation for horizontal accuracy

a preoperatively planned trajectory, we found that navigation was useful for guiding the endoscope to the sphenoid ostium, which was best seen with the surfacerendering CT. Inside the sphenoid sinus, the surface-rendering CT enhanced orientation by visualizing the sphenoid septations and its variations, especially in cases of complex sphenoid sinus anatomy with multiple septations or posterior sphenoethmoid air cells (Onodi cell, Figure 5A; multiple septations, Figure 5B) (54). To maximize the exposure of

Figure 4. Assessment of internal carotid artery (ICA) shifting: The distances between the ICAs of either side were calculated at well-defined points (1: posterior genu; 2: sagittal part; 3: anterior genu; 4: supraclinoidal ICA). Subtraction of pre- and postoperative ICA distances rendered the tissue shift.

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check. (B) Suction at indentation of the tuberculum sellae and (C) at indentation of the clivus for vertical accuracy check.

the tumor while preserving the ICA structures, the pituitary gland, and cerebrospinal fluid-filled cisterns, the optimal position of the opening of the sellar floor in relation to the tumor, gland, and arteries could be visualized on the navigation screen from a T1-weighted, contrast-enhanced MR and MR angiography (Figure 5) (35). During the sellar stage of the procedure, the parasellar tumor extension in relation to the ICA could be visualized (Figure 6), providing the surgeon important information for the safe and complete removal of the tumor. Accuracy Intraoperatively, the accuracy of neuronavigation was repeatedly evaluated by visualizing clinically relevant anatomical structures (Figure 3) (54). Apart from the case with intermittent patient tracker shift mentioned previously, the error always remained below the diameter of the suction (3 mm) in the advanced and standard navigation series. Tissue shift was measured by comparing the distances of the arterial structures on pre- and postoperative MR angiogram (Table 4). We observed a shift after tumor resection, which was largest at the segment of the posterior genu (2 mm; 0e9 mm); there was no shift at the anterior genu (0 mm; 0e3 mm) of the ICA. The shifting distance showed a correlation with tumor

volume, which was significant at all points measured except at the anterior genu. No correlation was found between spatial shift and the time interval following surgery to image acquisition of median 3 days (range 1e17). DISCUSSION Using latest generation navigation technique, we developed a protocol that for the first time adds a precise display of fine paranasal sinus structures to multimodality visualization during surgery and by continuous EM suction navigation provides a seamless integration into the operating workflow of endoscopic transsphenoidal surgery. Advancing Multimodality Imaging Although endoscopic surgery has many advantages, the ability to work in parasellar areas is fraught with the risk of potentially fatal carotid artery injury. To minimize this threat, intraoperative guidance has been described by numerous reports as a useful adjunct to endoscopic endonasal transsphenoidal pituitary surgery (8, 11, 16, 24, 34, 38). Not only in the experimental setting using cadavers (9, 16, 17, 52) but also in prospective clinical studies the practicability of neuronavigation with endoscopic pituitary surgery has been validated. Such

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Figure 5. (A) Complex sphenoid sinus anatomy with sphenoethmoid air cell. Considerable difficulty in removing the suprasellar part of the adenoma due to an unusually flat sella was reported. Standard navigation images (top) do not display the sphenoethmoid air cell seen on bone-windowed computed tomography (CT; middle, asterisk) that is separated from the sinus by a horizontal septum. Misinterpretation of the roof of the sinus leading to insufficient opening can create such intraoperative impression of a flat sella. Advanced multimodality navigation imaging (bottom) can

image guidance facilitates the surgical procedure by precise visualization of the spatial relationships between instruments and adjacent anatomic structures (18, 32, 37, 38, 55). Routinely, T1-weighted, contrastenhanced MR images are available in cases of endoscopic pituitary surgery. With the use of these images for navigation, the pituitary adenoma and its borders to the cavernous sinuses, the pituitary gland, and optochiasmatic structures can be visualized sufficiently (3, 5, 11, 24, 26, 27, 34, 35, 40, 50, 55). To differentiate between blood in the venous

improve intraoperative orientation by visualizing sphenoid septations. (B) Complex sphenoid sinus anatomy with multiple septations. Standard navigation images (top) do not display the complete and incomplete vertical and horizontal septations seen on bone-windowed CT (middle) that needed to be removed for sufficient access to the sellar floor. Advanced multimodality navigation imaging (bottom) can improve intraoperative orientation by visualizing sphenoid septations with equal detail as bone-windowed CT.

channels of the cavernous sinus and in the ICA, we superimposed an MR angiogram in red color-coding that displays the arterial vessels with high contrast (35). Because of its inability to directly visualize bone and because of the susceptibility artifacts of MR encountered at high-field strengths in the regions of the skull base, a CT scan is performed by many centers for assessment of the bony anatomy before endoscopic sinus surgery is performed. Bone-windowed CT has been described as helpful for navigation during the nasal and sphenoid phase of the approach (11, 16, 24,

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34, 38). Bone-windowing that is used to visualize fine bony structures on CT, however, visualizes soft tissue in a shaded way that it is not useful for multimodality image fusion for endoscopic sinus surgery. Therefore, we propose a new method of selective visualization of solid bone and fine paranasal sinus structures by using 2 different window settings of the same CT scan. The advantages of our method are 1) the transition between air and tissue is visualized by a thin line (“edge detection”) that displays fine paranasal sinus structures and openings of bone and mucosa; 2) the

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Figure 6. Assessment of tissue shift with pre- and postoperative (red contours) magnetic resonance angiogram. Nonfunctioning pituitary adenoma, volume 16 cm3, right parasellar extension Knosp grade IV. Additionally to the downward shifting of the anterior cerebral arteries and the supraclinoid ICA, a 9-mm inward shift of the posterior genu and sagittal part of the right internal carotid artery (ICA) is observed (arrows). Both ICAs are fixed at the anterior genu (asterisks).

underlying solid bone is displayed concurrently; and 3) the remaining image areas are kept transparent for overlay of soft tissue by MR. Therefore, this advanced multimodality image fusion is perfectly adapted to paranasal sinus and skull base surgery. Clinical Relevance of Visualization of Paranasal Sinus Anatomy Sphenoid Septations. Considerable variations exist in terms of extent of pneumatization of the sphenoid sinus (20) and the number and completeness of septations dividing the sinus cavity in chambers (52, 54). Complete septa have to be opened for sufficient access and unimpeded tumor removal. Complete and incomplete septations may be used as anatomic landmarks during opening of the sellar floor. Zada et al. (54) created a classification scheme based on the number of sphenoid sinus septations and their symmetry with respect to the vertical midline. Using coronary reformatted T1-weighted MR scans,

they encountered a “simple” configuration (0e2 symmetrical vertical septations) in 71% and a “complex” configuration (2 asymmetrical, more than 2, horizontal septations) in 29% of their study cohort of 156 scans. In comparison, our septum counts were slightly greater, possibly because we used dedicated CT surface rendering, not reformatted MR. We found a horizontal septum in 31% of cases and a posterior ethmoid air cell in 8%. Such anatomic variations can be a cause of incomplete exposure of the target area, resulting in limited ability to completely resect the tumor (Figure 5A). Incomplete resection at first surgery and consecutive tumor regrowth are the major causes of the endocrine and neurologic morbidity associated with this otherwise benign disease. Internal Carotid Artery. In our series, the median and most constant intersinus septum was deviating from the midline in 46% of cases, which corresponds to the cadaver series of Renn and Rhoton (44).

Table 4. Tissue Shift as Assessed by Changes in ICA Position Correlation Shift/Tumor Volume ICA Distances

Preoperative, mm

Shift (D Postoperative), mm

R

P Value

Posterior genu

21 (15e32)

2 (0e9)

0.6

< 0.005

Sagittal part

22 (13e33)

1 (0e8)

0.5

< 0.05

Anterior genu

20 (14e29)

0 (0e3)

0.4

NS

Supraclinoid part

15 (11e20)

1 (0e3)

0.5

< 0.04

ICA, internal carotid artery; NS, not significant.

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The deviated septum inserted as lateral as the ICA protruberance in 33% of our cases. Such deviation must be kept in mind when removing the bony septa to avoid damage to the underlying artery. If a wide opening of the sellar floor is desired, such as in case of a macroadenoma, the landmarks of the sphenoid sinus have to be interpreted correctly not to laterally damage the ICA. Such arterial injury that has been reported in less than 0.2% of cases in large series of experienced pituitary surgeons (13, 49) still contributes to the mortality associated with the procedure (39, 49). Neuronavigation provides intraoperative information about the anatomic variations that are possible risk factors for vascular injury: bony septal insertions overlying the ICA, low intercarotid distance (median 20 mm at the sellar floor in our series but can be as low as 4 mm (44) as so-called “kissing-carotids”), parasellar tumor extension with variable encasement of the ICA, or distorted anatomy from scar tissue in recurrent adenomas. The advantages of adding MR angiogram to navigation for transsphenoidal approaches to the skull base has been described by McGrath et al. (35). The relation between ICA and sphenoid sinus anatomy has previously been visualized with virtual endoscopy techniques (48, 53). A navigation system with the proposed advanced multimodality image fusion can provide prospective information about complex anatomic situations and thereby add to the safety of the procedure especially during extended approaches to the skull base, surgery of recurrent tumors, and large or invasive tumors that destroy the usual anatomic landmarks (16, 51, 54). Advancing to EM Tracking Technology Current standard navigation in most neurosurgical centers is performed with optic tracking (41). This technology is based on a tracking device (usually a straight probe with light-reflecting spheres) that is detected with an infrared camera bar as long as the field of vision between those is ensured. Although it is possible to enter the probe through the narrow endonasal corridor parallel to the endoscope, its tracking components are easily obscured by the endoscope arrangement and a continuous navigation is hindered. EM tracking, a technology that has long been used in the fields of ear-nose-throat

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and maxillofacial surgery, recently was reintroduced to neurosurgical navigation systems. The EM tracking technology is based on a magnetic field that represents the coordinate system and small coils that are brought into this field and serve as position trackers. Apart from the magnetic field generator, an EM navigation system consists—just like optic navigation systems—of a patient reference tracker attached to the patient’s head and a localization tracker for current position identification (22). The susceptibility of the EM technology to ferromagnetic interference with consecutive lower accuracy close to metal objects restricted its widespread use (1). Technological improvements, however, have overcome these initial limitations (46), and the latest generation of systems can detect the degree of metal interference and disable localization if expected accuracy falls beyond a critical threshold. Current EM systems have inaccuracies in the submillimetric and thus clinically safely applicable range (23, 33). Because of the limited size of the magnetic field (approximately 50 cm diameter) and the ferromagnetic susceptibility, a continuously stable EM navigation needs experience in setup and workflow. Using the setup proposed in this paper, EM navigation seamlessly translates into the neurosurgical approach: Continuous tracking without lineof-sight issue is the biggest advantages of EM systems over optic navigation. Further, the possibility of subsurface tracking provides the possibility to steadily navigate the tip of small flexible tools such as suction devices (14) and retain their accuracy even if the instrument bends during surgery. Using continuous update mode, the surgeon can display the actual position of the tip of his or her suction device throughout the whole procedure. This setup has been found a great advantage in terms of efficacy, as the recurrent exchange between working and tracking instrument disappears. There are economic cons of the EM technology, however: First, the single-use EM equipment adds considerable costs to the case, and the proposed navigation setup should therefore be reserved to recurrent or complex anatomical cases (10). Further, routine metal equipment such as skull clamps and nasal speculum cannot be used because of ferromagnetic interference. The

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skin-adhesive, patient-reference tracker may shift with tension on the draping what renders navigation inaccurate. The development of a minimally invasive patient tracker version that can be fixed to the patient’s head by a single screw via stab incision should be considered (18). Tissue Shift Compared with fluoroscopy, neuronavigation is based on preoperative radiological data that may become inaccurate due to tissue shift during surgery (40, 45). Updating these data intraoperatively is theoretically possible by the aid of an intraoperative MR (2, 7, 33, 36, 42). This, however, is costly and still not widely available. During surgical dissection, the patient’s anatomy is distorted and may shift after removal of the pathologic process. Neuronavigation visualizes preoperative scans and thus lacks intraoperative real-time image update. The tissue-shift is therefore not updated by the system and renders the navigation inaccurate. Tissue-shift is a well known issue during surgery for brain tumors (28, 43, 45); however, its impact on accuracy during surgery at the skull base seems much less due to the predominately nondisplaceable bony and dural structures. For transsphenoidal surgery, the extent of the tissue shift when removing sellar tumor tissue has not been defined yet but may be of major impact if medial shifting of the carotid arteries occurs after tumor resection. We therefore matched post- and preoperative MR angiographic images to calculate the extent of shift at various points in the course of the ICA. Part of the tissue-shift observed may be derived from a delayed movement of the anatomical structures postoperatively and may therefore irrelevant during surgery. A limitation of this study is caused by the time lag in surgery-to-postoperative MR angiogram caused by radiological capacity issues. Nonetheless, we did not find a significant correlation between the extent of the shift with the time interval between surgery and postoperative MR examination. According to our data, the initial accuracy remains high during surgery for the ICA close to the sellar floor. Caution has to be advised, however, for resection of parasellar tumor remnants at the end of surgery because our results show that there is a notable medial shift of the carotid segments that are located more distant to the

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dural ring/anterior clinoid process. Most tissue-shift was observed in patients with large and cystic tumors and may be attributable to the release of high intrasellar pressure when opening the basal sellar dura and/or resecting tumor. CONCLUSION Our advanced protocol provides seamless integration of navigation into the workflow of endoscopic transsphenoidal surgery by continuous EM instrument tracking. Image-fusion based navigation permits optimal visualization of bone, soft tissue and vascular structures during endoscopic pituitary surgery. Additionally, fine paranasal sinus structures can now be displayed concurrently. This improves orientation during the approach and may add to the safety of the procedure especially in cases of anatomical variations and in cases of recurrent adenomas with distorted anatomy. According to our data, the initial navigation accuracy remains high during surgery, especially for the ICA in the close proximity to the sellar floor. However, caution has to be advised for resection of parasellar tumor remnants at the end of surgery since we observed a notable tumor-volume dependant shift of the carotid segment located distant to the dural ring/ anterior clinoid process. ACKNOWLEDGMENTS The authors thank I. Dobsak for preparation of the figures, R. Teichman for continuing support with AxiEM electromagnetic navigation technology, and Yvan Paitel for support with Synergy Cranial 2.2 software. REFERENCES 1. Birkfellner W, Watzinger F, Wanschitz F, Enislidis G, Kollmann C, Rafolt D, Nowotny R, Ewers R, Bergmann H: Systematic distortions in magnetic position digitizers. Med Phys 25: 2242-2248, 1998. 2. Bohinski RJ, Warnick RE, Gaskill-Shipley MF, Zuccarello M, van Loveren HR, Kormos DW, Tew JM Jr: Intraoperative magnetic resonance imaging to determine the extent of resection of pituitary macroadenomas during transsphenoidal microsurgery. Neurosurgery 49:1133-1143; discussion 1143-1134, 2001. 3. Burkey BB, Speyer MT, Maciunas RJ, Fitzpatrick JM, Galloway RL Jr, Allen GS: Sublabial, transseptal, transsphenoidal approach to

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Conflict of interest statement: S. Wolfsberger is currently the educational consultant and technological advisory board member of the Medtronic Company. This study was in part funded by an educational grant of Medtronic Navigation. Received 18 September 2013; accepted 25 July 2014 Citation: World Neurosurg. (2014) 82, 6S:S95-S105. http://dx.doi.org/10.1016/j.wneu.2014.07.032 Journal homepage: www.WORLDNEUROSURGERY.org Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2014 Published by Elsevier Inc.

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