neurosurgical procedures in a 0.5 tesla, open-configuration

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Automedica, 2001, Vol. 00, pp. 1–35 © 2001 OPA (Overseas Publishers Association) N.V.Reprints available directly from the publisher Published by license underPhotocopying permitted by license only the Gordon and Breach Science

Publishers imprint.Printed in Malaysia.

NEUROSURGICAL PROCEDURESIN A 0.5 TESLA, OPEN-CONFIGURATION

INTRAOPERATIVE MRI: PLANNING,VISUALIZATION, AND NAVIGATION ∗

ARYA NABAVI a,b,c,f ,†, DANIEL F. KACHERa, DAVID T. GERINGc,d,RICHARD S. PERGOLIZZIa, WILLIAM M. WELLS III a,c,d,

TERRENCE Z. WONGe, CARL-FREDRIK WESTINa,c,RICHARD B. SCHWARTZa, PAUL R. MORRISONa,

NOBUHIKO HATAa,c, RON KIKINISa,c, PETER McL BLACK b

and FERENC A. JOLESZa,c,††

aDept. of Radiology, Magnetic Resonance Therapy,bDivision of Neurosurgery,cSurgical Planning Laboratory, Brigham and Women’s Hospital,

Harvard Medical School, Boston, MA;dAI Laboratory MassachusettsInstitute of Technology, Cambridge, MA;eDept. of Radiology,

Duke University Medical Center, Durham, NC;f Dept. of Neurosurgery,University of Kiel, Kiel Germany

(Received )

Computer-assisted 3-dimensional planning, navigation and the possibilities of intraoperativeimaging updates have made a large impact on neurological surgery. 3-dimensional renderingof complex medical imaging data, as well as co-registration of multimodal structural imagesand functional data has reached a highly sophisticated level. When introduced into surgicalnavigation however, this pre-operative data is unable to account for intraoperative changes(“brain-shift”). To update the structural information during surgery the scheme of intraoperativeimaging was put in place at our institution in 1995, with the installation of an open-configured,intraoperative MRI (Signa SP, 0.5 Tesla). In this paper the design, advantages, limitations andcurrent applications, (i.e., biopsies, craniotomies, and interstitial laser therapy) are discussedwith emphasis on the integration of imaging into the procedures. Furthermore we introduce ourintegrated software platform for intraoperative visualization and navigation, the 3D Slicer.

∗The work for this article was done while the first author (AN) was a visiting scholar at theDepartment of Neurosurgery at the Brigham and Women’s Hospital. His current address is:Department of Neurosurgery, University of Kiel, Weimarerstr. 8, 24106 Kiel.

†e-mail: [email protected]††Corresponding Author. e-mail: [email protected]

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New magnet designs and variations in utilization of present models characterize the rapidlygrowing field of MR-guided surgery. We provide our perspectives on future work.

Keywords: Image-fusion; Laser; Neuronavigation; Open-bore magnet; Neurosurgery

INTRODUCTION

In neurosurgery, the direct visualization of intracranial pathology is ofimmeasurable value for presurgical diagnosis and localization.

Before the 1920’s localization depended on indirect information. Preciseanalysis of the patient’s symptoms and thorough analysis of the clinical his-tory were and are a mainstay of topological diagnosis. Nevertheless directand indirect visualization of the lesion itself remained a diagnostic goal. Thedisplacement of the vascular tree (on angiography) [1] and the deformationof the ventricular system (on ventriculography) [2, 3] were the first methodsfor indirect visualization of the size and location of an intracranial lesion.More recently the integration of Computed Tomography (CT) and MagneticResonance Imaging (MRI) into diagnostic medicine has enabled direct visu-alization of intracranial lesions to determine size and location. With increas-ing image quality, initial working diagnoses are better established and smalllesions with atypical symptoms are now detected at earlier stages. In addi-tion to depicting structural anatomy, MRI sequences (i.e., functional MRI,dynamic perfusion studies, and diffusion weighted images) as well as SPECT(Single Photon Emission Computed Tomography), and PET (Positron Emis-sion Tomography) allow analysis of function and metabolism of the brainunder varying physiological and pathological conditions. There is increasingemphasis on combining different structural and functional imaging modal-ities in order to render a more complete picture of the brain. This objectivehas motivated the development of computer-assisted analysis, registration,processing, and visualization of medical images as three-dimensional render-ings of the brain [4–16]. Neurosurgery also underwent a technical revolutionwith the advent of operating microscopes [17] and bipolar coagulation [18].The operating microscope gives magnified surface visualization and opti-mal illumination of the surgical field, particularly for deep lesions. Bipolarcoagulation permits hemostasis with minimal damage to surrounding tis-sue, since current only travels between bipolar tips. The combination ofthese developments and subsequent improvement and adaptation of instru-ments and increasing microanatomical knowledge have given neurosurgery

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microneurosurgerical techniques, thereby decreasing the sizes of the neces-sary approach and improving outcome. Lesions within deeper brain areas,such as the brain stem, previously considered to be inoperable without thesetechniques are now removed with decreasing morbidity.

Kelly and Goers [19, 20] combined microneurosurgical techniques andneuroimaging studies, by introducing computer-assisted image-processingtechnique into stereotactic neurosurgery [19, 20]. Attempts to integrate func-tionality and precision resulted in highly specialized conventional stereotac-tic frames. Most of these frames obstruct free surgical access during tumorresections. To allow more access lighter frames have been constructed. Itis feasible, to consider the fiducials, commonly used in frameless stereo-tactic navigation, as the ultimate miniaturization of that external referencesystem [22, 23]. Through stereotaxy [19, 20, 23], computers have been intro-duced into neurosurgical procedures. Between 1986 and 1995, several groupsdeveloped so-called “frameless” stereotactic systems [11, 24–36]. Thesesystems provide the surgeon and patient with precise guidance without theobstruction and discomfort of frame application [23, 37] improving neuro-surgical efficiency and surgical technique.

The major shortcoming of both frame-based and frameless stereotacticsystems is their use of presurgical data. As surgery progresses, intraop-erative changes and deformations occur, commonly referred to as “brainshift” [38–47]. These changes are due to tumor resection, swelling, andCSF drainage. As these processes are unavoidable in the course of neurosur-gical procedures, they progressively reduce the accuracy of neuronavigationsystems relying on preoperative data. These changes occur mainly duringcraniotomies for tumor resections, but may alter the accuracy of stereotacticprocedures for biopsies as well [41]. The “brain shift” problem has ultimatelyled to the development and refinement of pre-existing imaging techniquesfor intraoperative use. Two-and three-dimensional ultrasound, CT and MRIwere integrated to acquire volumetric images [48].

Although the image quality of intraoperative ultrasound has improved[49–52], it provides inferior information to MR [38, 42]. Use of CT, eitheras a stationary [53, 54] or mobile unit [55], has the disadvantage of radiationexposure, and soft tissue discrimination is inferior to MR. Comparingthe potential of various imaging modalities for intraoperative imaging,MRI presents an unequaled range of capabilities. Multiplanar imagingcapabilities, high contrast, spatial resolution, and high sensitivity areparticularly useful for intraoperative guidance. Conventional T1 and

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T2-weighted (T1-w and T2-w) sequences detect various abnormalities withinthe brain. Specialized sequences like dynamic gadolinium-enhanced imag-ing [56, 57], optimized gradient-echo sequences for early identification ofblood products [58–60] visualization of blood-flow in limited resolution(TOF and phasecontrast angiography) (unpublished data) and phase-basedtemperature changes for thermal ablation [61] are available on the intra-operative 0.5 Tesla system in our department. Additional information suchas the orientation of white matter tracts (tensor representation of diffusionweighted images [62]), cortical function (fMRI), and spectroscopy are onlyavailable on higher-field conventional and interventional magnets [63–67].

Presently a variety of intraoperative and interventional MRI scanners, withvariable access to the patient, can be applied for intervention ranging frombiopsies to open surgeries [68–71]. In 1993 when the decision for the devel-opment of an open-configuration intraoperative MRI was made at our institu-tion, in collaboration with GE, the involved parties decided to design a scan-ner, which combines the imaging and surgical spaces. We will discuss thevarious contemporary MR-scanner designs with special emphasis on our sys-tem and our approach to presurgical planning and intraoperative navigation.

3D VISUALIZATION AND IMAGE-FUSIONFOR SURGICAL PLANNING

Preoperative surgical planning starts with data acquisition with optimumspatial and contrast resolution using a 1.5 T MRI scanner. The patient under-goes a standard protocol, which includes a 3D-SPGR (spoiled gradient echo)volumetric MRI-acquisition (124 slices 1.5 mm) and phase-contrast MRangiography. These acquisitions are used to identify and segment the rel-evant anatomic structures and to render a 3D surface representation of thepatient’s pathology [7]. A standard model includes the patient’s skin, brain,cerebral ventricles and vessels, as well as the lesion [4, 5, 7, 72] (see Fig. 1).

Imaging modalities representing various anatomical, (CT, MRI: T1-w, T2,SPGR, proton density, diffusion weighted, and phase-contrast MR angio-graphy) and physiological as well as pathological (SPECT: Single-PhotonEmission Tomography; PET: Positron-Emission Tomography; fMRI: func-tional MRI) characteristics, are abundant (see Fig. 2 for multimodal imageinformation). Their different diagnostic yield makes their combined visual-ization for comparison and evaluation desirable [8, 9, 12, 73–76]. This data

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FIGURE 1 Presurgical planning: Clockwise starting upper left: 1. Orthogonal grayscaleswith surface models for vessels (MRA), tumor (green), and Thallium uptake (red wire-frame).2. Opaque tumor model, note the incongruent areas of tumor and thallium model. 3. Translucentbrain model is added. 4. Skin as a reference model.

is neither acquired at the same time, nor in the same coordinate system. Thebasic problem of multimodal image information is the registration of suchdata into a common coordinate system [8, 9, 14, 74].

There are two basic approaches to co-registration: the application of exter-nal fiducials, or the utilization of patient specific features [9, 13, 14, 75]. Ourapproach is to use the entire patient specific information in a volume-to-volume registration using an algorithm, applying maximization of mutualinformation (MMI) [10]. The final goal of surgical planning and simulationis to incorporate these techniques into intraoperative image-guidance [77].This integration requires the rigid body transformation of the presurgicaldata (image space) to the patient (physical space) in surgery [30]. With com-puter assisted navigational tools, the patient’s anatomy can be visualized as2D or 3D representations in relationship to the position of tracked, hand-heldinstruments within the surgical field [11, 24–36].

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FIGURE 2 Multimodal image information (graphical user interface of the 3D Slicer[15, 16]:Image fusion using the presurgical structural MRI, MR Angiography and SPECT (Thallium andTechnetium). The image shows a cutaway of the skin model. The cut-planes are the reformattedgrayscale images. The Thallium-SPECT is depicted as a red wire-frame. The blue and red showthe Technetium SPECT activity, which is related to the blood flow (red: areas with the highestblood flow; blue: intermediate blood flow; no color: no SPECT activity).

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Within the open MRI, presurgical data can be used for planning trajectoriesand approaches. The data is aligned to the patient positioned in MRT (Mag-netic Resonance Tomography) [15, 16, 78]. These models become inaccurateas surgery proceeds. Algorithms to deform the presurgical data, for exam-ple to compensate for the intraoperative shift of functional areas, are beingtested, but are not yet applicable for routine use [45, 79–81].

It should be emphasized that image acquisition, display, and visualizationin the operating room are different from diagnostic situations. Surgical neces-sities limit the time available for intraoperative imaging. To be fully inte-grated into the procedure, acquisition and display of intraoperative data haveto be dynamic and primarily driven by the surgeon. Therefore we integrateda localization system, and more recently a computer-assisted navigation andvisualization system, the 3D Slicer into the Signa SP [15, 16, 78].

DESIGN AND IMPLEMENTATIONOF THE OPEN-CONFIGURATION MRI

The development of a vertical gap mid-field strength MRI system (0.5 Tesla,Signa SP) began in 1993 [6], as a collaboration between General ElectricMedical Systems (Milwaukee, WI) and the Brigham and Women’s Hospital.The guiding concept stated that the scanner should give access for open cran-iotomies while being able to acquire MRI studies during procedures withoutmoving the patient [6, 48, 82–84]. This design presented various engineeringproblems. A fully magnetically shielded surgical-MRI suite had to be built,including a patient holding as well as service area [85]. MR-compatibletools as well as anesthesiological equipment were needed. This includedsurgical instruments, a carbon fiber Mayfield head holder, flexible Book-walter retractor, Midas Rex drill, cortical stimulator, ultrasonic aspirator,monopolar and bipolar electrosurgical units, operating microscope, venti-lator, patient monitor, intubation handles and blades as well as peripheralnerve stimulator, and more recently SSEP and EEG equipment [83, 86–88].MR-compatible equipment is now readily available [89–91].

Access to the patient was achieved by designing the superconductingmagnet with coils in two separate communicating cryostats with a gap at thecenter of the magnet. Our prototype has a 56 cm gap providing a sphericalhomogeneous (30 cm diameter) 0.5 T static field in the center of the openbore [6]. This gap gives sufficient access for open surgery, although the

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surgeon’s mobility is restricted. The scanner console and the workstations,for image-guidance and image processing, are situated outside the shieldedMR room. The neuroradiologist reviews the acquired images on the diag-nostic console, displaying them to the surgeon on LCD flat panel screenswithin the scanner bore, communicatingvia intercom.

Coils needed to be designed, which could be flexibly incorporated intothe sterile surgical draping, while giving access to the region of treatmentbeneath the coil [91].

The patient can be positioned within the scanner in two ways: (1) pass-ing through the bore of the scanner or (2) perpendicular to the axis of thebore with the patient passing through the gap at the center of the scanner(side-dock). With position (1), two surgeons have access to the patient, fromeither side. Although the “side-dock” position provides space for only onesurgeon, it yields more access to the patient when in prone position, anapproach for posterior fossa and occipital lesions. The microscope is intro-duced over the surgeon’s shoulder. Positioning must be carefully planned.Sterility is a major issue with the introduction of any large device into theoperating field, or, as in our case, the operating field into the device. Never-theless, the potential increase in infection risk, related to patient transportsis eliminated [58].

“Near Real Time” Interactive Imaging

One of the initial design premises of the Signa SP was to enable the sur-geon or interventionalist, to define the acquisition plane needed for imageguidance [6, 92]. For this purpose, a 3D-digitizer system (Flashpoint 5000,Image Guided Technologies, Boulder, CO) was installed as an integral partof the SignaSP. It consists of three charge-coupled device (CCD) camerasand a locator with three infrared light emitting diodes (LEDs) [30, 37]. Aneedle is inserted through a hole in this star (see Fig. 3). Fixed to a specificdepth, the needle’s tip can be localized and tracked. The locator position andorientation are updated at a rate of 10 Hz. The coordinates are calculatedby a workstation (Sun Microsystems, Mountain View, CA) and can be usedto define an imaging plane. Images acquired in plane (0 or 90 degrees) orperpendicular to probes or instruments are displayed on the in-bore moni-tors, providing visual feedback. Depending on the elected pulse-sequencean image is updated within 3–24 seconds. After adjustments, the scannerneeds the allotted time, to create an image. If the locator is moved during

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FIGURE 3 Localizer: After craniotomy the 3 LED hand-piece with the probe is held inposition. The tip of the probe touches the brain surface (arrowhead). The coordinates for theprobe’s tip are given by the plane of the three LEDs (arrows) and by the preset depth of the probe.

the acquisition, a new plane is automatically defined, blurring the acquiredimage. Faster sequences were developed and implemented such as SSFSE(single-shot fast spin-echo) providing T2-weighted images, acquired every 4seconds. The trade off for fast imaging is reduced image quality (see Fig. 4).Used routinely for biopsy procedures, the optical navigation system can besimilarly utilized to position catheters or needles (e.g., for cyst evaluationor drainage [93]), or to place thermal ablation probes. Although the combi-nation of the Flashpoint system with the SignaSP is helpful for localizationand guidance, it is too time-consuming to use it during open craniotomies.

The 3D Slicer: Integrated Interactive Image Guidance

The 3D Slicer, a program developed in collaboration with the AI-Lab at theMassachusetts Institute of Technology (MIT) [15, 16] integrates presurgical

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FIGURE 4 Comparison of“ real-time” and 3D Slicer visualization for biopsies: From left toright: Image 1 and 2 show two adjacent real-time images. 1. shows the needle tip (black arrow),and 2. shows more of the canula (black arrowheads) of the biopsy needle. The target is visualized,but the surrounding tissue is blurred. 3. shows a 3DSlicer display recorded simultaneous to the“real-time” images (1 and 2). This T2-w image has a slightly different angle, but delivers moredetail than the “real-time” image. Noteworthy is the proximity of the internal carotid artery(ica= internal carotid artery).

planning, 3D visualization and computer-assisted navigation with updatedintraoperative images. It provides capabilities for image editing, model gen-eration and registration of multimodal presurgical (see Figs. 1 and 2) (MRI,CT, SPECT, phase contrast MR Angiography, functional MRI) and intraop-erative studies. The 3D Slicer has a modular, extendable design. Its graphicalinterface utilizes OpenGL, Visualization Toolkit (VTK) [94], and the Tcl/Tkscripting language [95].

The SignaSP console and imaging workstation are connected by networkto a visualization workstation (Ultra 30, Sun Microsystems, Mountain View,CA) running the 3D Slicer. The 3D localizer’s position is transferred tothis workstation. The peak transfer rate between the two workstations is10 MB/s. As soon as intraoperative updates are acquired, they are trans-ferred to the workstation and loaded into the Slicer. Since the patient hasnot moved between image acquisition and navigation, the image coordi-nates (image space) correlate with the patient (physical space), withoutregistration. The surgeon can investigate the surgical field immediatelyusing the locator. The corresponding updated image is displayed on thein-bore monitor with a virtual locator representation in a user-specifiedplane. The surgeon, using the pointer as a 3D mouse, can scroll throughthe images, selecting his region of interest. Furthermore the plane of viewcan be arbitrarily changed, according to the angle of the locator in space,thus yielding axial, sagittal, coronal or arbitrary planes in the direction ofthe probe.

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CLINICAL APPLICATIONS

Since 1995 a variety of procedures were carried out in the intraoperativemagnet (see Tab. I). Although the initial applications were primarily per-cutaneous biopsy [92], the capability ultimately encompassed a broad rangeof interventional and surgical applications [47, 56, 58, 61, 83, 85, 86, 93, 96].The SignaSP has been used to guide neurosurgical procedures, includingbiopsies, open craniotomies, transsphenoidal pituitary and spinal (cervicaland lumbar) surgery.

The neurosurgical applications encompass 320 craniotomies for lesionresection and more than 100 biopsies. The pathologies most frequentlytreated with open craniotomies were low-grade glioma (astrocytoma I-II:42), oligodendrogliomas (n=40), oligoastrocytomas (n=22), anaplasticastrocytomas (Astrocytoma III: 22), glioblastoma (n=64) and recurrent pre-viously treated Glioma (n=43) [97].

Although serial biopsies of lesions on CT and MR [21] as well as autopsystudies [98, 99] have shown, that tumor cells exist outside of the imagedlesions, Bergeret al. found a significantly better prognosis for low-gradeastrocytomas [100] as well as oligodendrogliomas after gross total resection.Although treatment of low-grade gliomas in adults remains controversial[102] our approach to these lesions is to attempt a gross total resection ofthe signal abnormality in all cases. The sensitivity of MRI for low-gradelesions in conjunction with intraoperative navigation is crucial to achievethis goal. Resection is particularly challenging in close vicinity to criti-cal brain structures. Patients with lesions adjacent to highly specializedregions (in our groupn=61) are operated under conscious sedation which

TABLE I Number and type of procedures performedin the open-configuration MR (Signa SP) at theBrigham and Women’s Hospital as of December 1999

Sinus Endoscopy 12Prostate Brachytherapy 80Breast Lumpectomy 8Liver Cryotherapy 10Brain Laser therapy 9Spine Surgery 17Pituitary Tumors 10Biopsies 110Craniotomies 320

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allows neurophysiological (e.g., speech, movement and memory tasks) andelectrophysiological testing. A vital tool for such cases is an electrical corti-cal stimulator (“Ojemann”-Probe, Radionics, Burlington, MA) [103–105],which is used to localize specific brain function in the conventional OR[106] and was modified for use in a magnetic field [91]. For lesions, whichborder directly or are surrounded by eloquent tissue [107], the combinationof imaging and electrophysiology allows the maximum possible resectionof the signal abnormality while [101, 107] avoiding neurological deficits.

Anaplastic astrocytomas and glioblastomas are commonly referred toas high-grade glioma [97]. They progress more rapidly, than low-gradelesions. These malignant tumors destroy the blood brain barrier (BBB).Contrast agents, such as gadolinium-DTPA, extravasate where there is sucha disruption, causing enhancement of the tumor. Initial gross total resec-tion of the contrast enhancing area shows significant benefit regarding timeto recurrence, survival and quality of life [108–110]. Intraoperative guid-ance has been shown to increase tumor resection significantly as comparedto neuronavigation alone [47, 58, 111, 112]. The neuroradiological evalu-ation of recurrent tumor growth is difficult. Particularly distinguishing activetumor from radiation changes (such as necrosis, hypervascularisation, whitematter changes) can be almost impossible on conventional contrast enhancedMRI. “Dynamic MRI” (see Fig. 5), determines the temporal resolution ofcontrast enhancement and distinguishes highly and less active regions (e.g.,cysts, necrotic areas) in malignant tumors [56, 57]. Following rapid bolusinjection of gadolinium two-dimensional fast spoiled gradient echo (FSPGR)images through the tumor volume are acquired. Tumor recurrence, with asso-ciated neovascularity, enhances early, while post-treatment necrosis showsdelayed enhancement. An additional study, which aids in the differentialdiagnosis of active lesion and radiation necrosis, is SPECT (see Figs. 1 and2) [74, 113–115]. With image fusion of presurgical SPECT to the intraop-erative images in conjunction with the results of the dynamic study, activeregions can be better localized for biopsies or resection.

MRI-guided Biopsy

Biopsies were the main applications of intraoperative MRI at our institu-tion before instrumentation for craniotomies became available. At presentthey account for 10 to 20 of the intraoperative MR-guided cases per year atthe Brigham and Women’s Hospital. Our main indications for MR-guided

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FIGURE 5 Dynamic study in a recurrent glioblastoma: This series of six consecutivescans (1–6) shows the different contrast distribution as can be seen on following the accu-mulation of the gadolinium-DTPA. The first image (1) shows the baseline scan, beforeGadolinium-Administration. The following 4 scans show the gadolinium accumulation, earli-est in the posterior portions (arrow in 3). The anterior ring enhances later (arrow in 4). Thefinal image (6) shows the contrast enhancement after a few minutes. In this last image it isimpossible, to distinguish with different time courses of Gadolinium enhancement.

biopsies are small diffuse lesions, radiation changes with inconclusive imag-ing studies to rule out recurrent tumor growth, and lesions close, or withincritical structures (e.g., brainstem). The prime objective in biopsies is tofind the least harmful trajectory to obtain a definite tissue diagnosis. Thepatient’s head is always fixed in a 3-point head-holder (Mayfield). The MRimaging sequence best defining the target tissue can be selected for imageguidance. A baseline set of conventional 2D images is acquired, identify-ing the target. Furthermore a 3D-volume acquisition provides better spatialorientation (see Fig. 6). Since the depth of the needle can be set arbitrari-ly, we use the 3D Slicer’s virtual tip, to explore the suggested needle path.Once the trajectory is defined, a burr hole is placed at the specified location.The trajectory is again verified and the localizer fixed in this position with aself-retaining Bookwalter retractor, attached to the Mayfield. Other fixationdevices include burr-hole mounted arrestable needle guides [91, 116, 117].

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FIGURE 6 Biopsy using the 3D Slicer: The 3D Slicer allows selection of various imagetypes for planning approaches. 1. The composite of the intra-procedural T2 and SPGR imageshows the target of the biopsy, best seen on T2. The SPGR is needed to define the trajectorywhile displaying the anatomical surrounding. 2. This visualization of T2 axial and reformattedsagittal image allows a more thorough appreciation of the spatial extend of the lesion, but doesnot display enough information to plan the trajectory.

FIGURE 7 Real-time biopsy: From left to right: The planned trajectory is depicted as a brokenline. The signal void depicts the advancing biopsy needle at consecutive scans. The needleartifact exaggerates its real diameter. Subsequent conventional scans are less susceptible, andprovide verification of the final position.

Fixation keeps localizer and trajectory constant throughout the procedure.While advancing the probe we track the needle path (see Fig. 7). For enhanc-ing lesions, T1-w contrast-enhanced fast spin-echo (FSE) images are used(updated every 14 seconds). For non-enhancing lesions, T2-w FSE images(update every 15–24 seconds), and single-shot fast spin echo (SSFSE) areacquired every 4 seconds.

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Once in the target area, needle position within the signal abnormality canbe additionally confirmed with conventional 2D scans, and subsequentlythe biopsies taken. This procedure verifies that the biopsy is taken from theobserved tissue abnormality, ruling out incorrect targeting as a reason fornon-diagnostic neuropathological reading. If indicated, a laser fiber can beintroduced for thermal ablation of the targeted region (see Interstitial LaserTherapy of Intracranial Lesions). After withdrawing the needle, control scansare acquired, to rule out complications [83, 86, 92].

MRI-guided Craniotomy

At our institution most procedures for the resection of brain tumors are con-ducted under general anesthesia. Patients with tumors in critical brain areassuch as motor or speech cortex undergo open craniotomy under conscioussedation (n = 61). After the patient is positioned and the head rigidly fixed, aflexible MRI-surface coil is applied to the region [58, 91]. An initial baselineset of 2-dimensional slices is obtained through the volume of interest, priorto incision, chosen according to the imaging characteristics of the lesion. Theimaging plane is oriented to best visualize the lesion, the expected approach,and areas to be preserved (critical areas:e.g., motor and speech cortex). Weattempt to keep our sliced-based acquisition as close to true axial, coronal orsagittal as feasible. The use of these familiar planes facilitates orientation,relocalization and identification of critical anatomic structures as the surgeryprogresses. Once these settings have been loaded into the MR console, cor-responding orthogonal image slices are acquired by rescanning. As imagingis repeated at intervals during the surgery, serial comparison allows verifi-cation of the current location in relation to remaining tumor and adjacentcritical areas [47, 58] (see Tab. II for pulse sequences routinely used in opencraniotomies).

After the baseline scans, a 3D volume scan of the patient’s head isacquired. This scan is transferred to the workstation running our navigationsoftware. As the localizer is moved within the surgical field, the computerreformats these slices at the stylus-selected position. The surgeon may usethis tool to navigate through the image volume, in order to define the bestapproach to the lesion (see Fig. 8). For high-grade lesions we perform thedescribed dynamic scan after dural opening. Following significant intraoper-ative changes, further imaging updates are acquired. These changes referredto as “brain-shift” (see Fig. 9, bottom row), commence with the cortical

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TABLE II Pulse sequence parameters for the scans mentioned in this article

T1 T2 Dynamic SPGR

TE (MS) 29 85 4.3 12.3TR (MS) 600 400 13.8 28.6BW (kHz) 6.25 6.25 6.25 7.2Thick (mm) 5 5 6 2.5Spacing (mm) 1 1 0 0Resolution 256× 128 256× 128 128× 128 256× 128NEX 2 1 1 1# images 12 12 70 60Time [min] 2.05 2:34 2:00 3:55

FIGURE 8 Setting a trajectory with the 3D Slicer: From left to right the skin has graduallybeen faded out, to show the underlying grayscale plane used for navigation. The skin wasreconstructed from the intra-operative scan. An in-plane view in the trajectory of the probe isvisible. The tip of the probe is on the dura, after craniotomy. This plane is visible within thereference frame of the patient’s skin, to facilitate orientation.

sinking after cerebrospinal fluid drainage and subsequently increase duringtumor resection [39, 41, 43, 44]. It is important to realize that intraopera-tive deformations are a dynamic event [46]. Sporadic intraoperative imag-ing can very well miss aspects important to mathematical simulations ofthe overall brain shift [41, 44, 45, 79, 118, 119, 120, 121]. We observe sub-stantial intraoperative changes within 30 minutes. In our opinion frequentintraoperative update is warranted to detect these changes. Integrated intoour navigation system, these updates correct for intraoperative deforma-tions [80, 81]. Prior to imaging, electrical equipment and ferrous-metallicinstruments are removed from the surgical field. These devices can producesignificant imaging artifacts if left in the scanner. The operating microscoperemains in position.

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FIGURE 9 3D Slicer navigation for resection control: In this case an oligodendrogliomawas removed from the frontal lobe (see bottom row). The upper row shows the 2 screen saveswhile the surgeon is probing the resection cavity. From left to right: axial, and combination ofaxial and saggital slice from a different angle, providing a spatial impression. The bottom rowshows how the 3D Slicer facilitates direct comparison of various intraoperative acquisitions.The display shows 2 different time points, after dural opening 1 and after tumor removal 3. Inthe middle an overlay of both simulates the motion during resection by fading from 1 to 3. Thisability is very useful in comparing “spreading enhancement”. Note the intra-operative change(“brain shift”) with surface sinking and ventricular shape change.

Intraoperative imaging may be frequently employed, to verify stages ofthe resection (see Fig. 10). Our imaging frequency ranges between 5 and 10serial acquisitions (10–12 images) during the resection more frequently inthe vicinity of critical brain areas. Early detection of complications, such ascontralateral bleeding (one patient developed a contralateral hematoma) orbleeding into the resection cavity may be resolved before clinical symptomsdevelop [58].

Contrast Dispersion “Spread Enhancement”

If indicated, we administer gadolinium after dural opening. In some cases,particularly in high-grade or recurrent gliomas, diffusion of contrast beyond

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FIGURE 10 3D Slicer navigation during resection: From upper left to lower right. Thissequence of 4 still images shows the display the surgeon sees on the in-bore monitor. The probe(white bar) is used to delineate the present surgical cavity. The surgeon follows the outlines ofthe cavity with the probe, starting in the posterior end (1st image) bottom and anterior portion.The scan remains in the chosen orientation (axial plane) but the level changes according to theprobe’s position, as can be followed by the change in the ventricle cuts.

the original enhancement blurs the tumor boundaries. The effect appearsto increase with the length of the procedure suggesting continuous con-trast leaking from the vascular compartment. Generally the initial contrastenhancement remains more defined, whereas the area of dispersion is lessintense. This may allow a reasonable distinction between the original tumorboundary, and the spreading enhancement. It is commonly observed thatcontrast as well in CT as on MRI diffuses into surrounding regions overtime [122–124].

Knauth gives an excellent discussion and experimental data of surgicallyinduced enhancement patterns [125]. In our overall clinical practice, weencountered the dilemma of neuroradiologically undefinable tumor marginsin only one case. This patient was post-radiation and showed pronouncedintensity changes of most of his ipsilateral hemisphere within 1.5 hours aftercontrast administration.

The development of new intravenous contrast media [126, 127] continuesto yield ambiguous results (i.e., not tumor specific). Nevertheless, contrastmedium, which selectively marked tumor cells, could potentially improve

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intraoperative MR visualization of resection and tumor margins, as well asextent of resection without spreading enhancement.

Interstitial Laser Therapy of Intracranial Lesions

Interstitial laser therapy (ILT) for thermal ablation has been extensivelystudied over the past decade [128–131]. Nevertheless its clinical applica-tion is still experimental and has not been integrated into clinical routine[61, 132–135].

The principle of LIT is to apply temperatures of 50–60◦C in order toinduce cell death. Since this temperature induces cell death in both neo-plastic and normal cells, accurate stereotactic targeting and close onlinemonitoring of the disseminating heat are essential. MRI is sensitive to tissuechanges induced by temperature and may be used to monitor the dose deliv-ery [136–142]. The ablation of tissue, the denaturation of proteins, dehy-dration, and edema all induced by the laser can be visualized on intra-andpost-procedural T1, T2-weighted, and SPGR images.

Proteins begin to denature at 41◦C, though the target temperature for clin-ical applications is in the 50–60◦C range. In the brain, temperatures closeto 100◦C should be avoided. Laser dosimetry is complicated by the brain’sheterogeneous histology (i.e., densely or loosely packed cells, abundanceof fibers, or vascularity) which is associated with variable heating charac-teristics [143, 144]. Therefore, software for the online monitoring of ILTwas developed [144, 145]. Our ILT software runs on the same intraoperativenavigation workstation discussed above [96].

ILT indications at our institution are small deep lesions, especially thosein close proximity to critical brain areas or patients who did not wish opensurgery. In the literature applications for low- and high-grade lesions havebeen reported [132–134, 146]. Experimental as well as clinical designs forthermal monitoring have been investigated on 0.2 [147, 148], 0.3 [149], 0.5[61, 150], and 1.5 [144, 151, 152] Tesla Magnets. Our intraoperative MRIcombines the functions for stereotactic definition of target points and tra-jectories (3D Slicer) as well as online monitoring of the applied energy intoone tool. Laser ablation is preceded by biopsy for cytologic confirmation ofpathology. Subsequently a laser fiber is introduced into the lesion along thesame path of the tracked biopsy instrument. A “test” impulse is applied forabout 1 minute, which allows verification of the laser fiber tip position withT1-w images, by “T1-subtraction”. T1 subtraction utilizes the changes inpixel intensity of the treated lesion, which decreases linearly as temperature

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FIGURE 11 Subtraction of T1-w images to visualize temperature change: We use T1-subtraction to verify the tip position in interstitial laser therapy. T1-w images are acquiredduring the heating. These scans are subtracted from baseline scans (pixel subtraction). Thedifferences are color-coded. These consecutive images covering 90 seconds show the image (1)immediately before, and during energy deposition (30 seconds and 60 seconds after starting theimpulse). Note the color change from green to orange to red, visualizing the rising temperature.

FIGURE 12 Phase mapping for the visualization of temperature change: From left to right:1. Pre-ablation baseline image. 2. Following 2 minutes of energy deposition where hypointensesignal documents the tissue reaction. 3. Phase mapped image of the proceeding two, displayingthe center of the sphere as hotter than the periphery, which fades into the surrounding tissue, asthe temperature levels sink to normal.

increases from 37–50◦C [140, 153–155]. Beyond 50◦C, metabolic changescaused by the denaturation, prevent absolute temperature estimation fromMR-imaging. By subtracting the most recently acquired image during energydeposition from a baseline scan, a color-coded “difference image” may begenerated (see Fig. 11). This visualization technique also verifies locationand positioning of the fiber tip [61, 96, 156].

Following fiber position verification, a “treatment” impulse is appliedfor 5 minutes [152]. The thermal change is visualized by “chemical shift”imaging. Temperature changes cause a chemical shift in the resonant

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frequency of water protons [157, 158]. This in turn will cause a detectablephase change, in SPGR pulse sequence [145, 159, 160]. To conclude the pro-tocol, we acquire another 3D-volume data set after contrast administration(see Fig. 13), rendered as a 3D model (Fig. 14). Neuoradiologic follow-up

FIGURE 13 Post-ablation gadolinium enhanced study: Two adjacent slices of the final3D-volume SPGR. The patient is still in the MRI. The laser fiber is visible as signal void,running into the tumor from upper left. Primarily non-enhancing there is contrast uptake aroundits periphery, with a central non-enhancing region.

FIGURE 14 3D visualization of laser treatment effects: 1. Transparent surface model of thebrain, with tumor (green), ventricles (blue) and laser fiber (yellow): 2. The red sphere showsthe treatment effect (70% of the lesion). The treated area overlaps with the superior tumorboundary. Energy deposition was to be discontinued, to preserve adjacent critical tissue.

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has shown the lesions to first enlarge over a 12 months period and finallycollapse [134]. More precise knowledge of tissue-specific heat conductivityand more accurate simulation software will be crucial for future progress.

DISCUSSION

Our experience has proven intraoperative MRI to be a valuable and oftenindispensible neurosurgical tool. Imaging flexibility and contrast is wellsuited to guide neurosurgical procedures [47, 58, 83]. Furthermore, the inte-gration of a computer-guided navigation system combines the qualities ofinteractive navigation with the advantages of consistently available imageupdates [15, 16, 78]. Further advancements are the implementation of MRIcompatible electrical cortical stimulators for the electrophysiological testingduring craniotomies in awake patients (conscious sedation). There is com-mon consent in our institution, that the ability to acquire frequent updates ondemand during resection as well as the capability of navigation are worth theinconveniences of the limited space, restrictions in positioning, and limitedimaging armamentarium. The surgeon can verify his planned approach andprogress. Surgical strategies can be reevaluated, if warranted, by updatedinformation. Intraoperative deformations (brain shift) [46, 80] and changesin contrast enhancement are seen with the routine use of intraoperativeimaging.

Since the first design and implementation of the “double-doughnut” atour institution, various designs were modified and introduced for surgicalinterventions [68–71].

Tronnier, Wirtz, and colleagues (Heidelberg/Germany) have demonstratedthe feasibility of a horizontal gap open-configuration 0.2 Tesla MRI system(Open Viva, Siemens AG, Erlangen Germany) for neurosurgical interven-tions [40, 120, 161]. Not intended as a dedicated surgical scanner [121], theopening allows access for interventional procedures, such as MR-guidedbiopsies. For surgery the patient has to be moved out of the scanner. Trans-porting the patient between an adjacent conventional OR and the shieldedMR suite allows minimal changes to the conventional neurosurgical proce-dure and instruments. Significant engineering challenges have been over-come in the Siemens Open Viva. Head holder and table were modified toallow transport and docking to the MR scanner [40, 120, 121, 162]. The

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logistics of moving the patient are elaborate, and do not permit frequentimaging. Recent modifications of the suite overcome this issue. The patientis positioned outside of the scanner’s sensitive field. The table can be rotated,to move the patient’s head into the scanner [163]. This magnet design hasthe widest distribution in clinical centers.

A variation of this design, a horizontal gap GE Signa Profile (0.2 Tesla)flipped vertically, was installed at the University of Toronto Medical Center(Canada). The patient can be accessed through a 47.1 cm wide gap or moved1 m past the outer edge of the magnetic field, permitting use of conventionalferrous instruments. A navigation system is integrated for updated imageguided surgery.

The 0.12 Tesla table mounted low-field scanner (Odin Technologies)presents the opposite extreme of high-field intraoperative magnets. There areno compatibility problems with current neurosurgical instruments. The mag-net is lowered beneath the operating table, until needed. However, the imagequality of this device might not be sufficient for neurosurgical procedures.

In Minneapolis (Minnesota) a short bore design (Philips GyroscanACS-NT; Philips Medical Systems, Best, The Netherlands) has been installedfor neurosurgical procedures [64, 67]. The operative procedures takes placeoutside the 5 gauss line, permitting the use of conventional OR instruments.For imaging, the table is docked to the gantry, and the patient moved intothe bore. Since it is a high field magnet, ferromagnetic material has to beremoved prior to imaging [164]. Patients undergo craniotomies under gen-eral anesthesia. Biopsies can be taken with an extended arm, while the patientis in the scanner [116, 165].

In Calgary (Canada) a mobile, ceiling mounted 1.5 Tesla magnet (Mag-nex Scientific, Abingdon, Oxon, England) has been implemented [65, 66].The magnet is brought into the OR on demand, on ceiling mounted rails(“overhead crane technology”). The building is designed to allow operation,emergency, and standard radiology suites to share the magnet. The oper-ating table is MR-compatible. Furthermore a special removable coil, moreresembling the cage on a conventional scanner was implemented. The twohigh-field magnet designs as implemented in Minnesota and Calgary offer afull range of imaging studies (e.g., Spectroscopy, fMRI, Diffusion weightedimages, MR angiographies). Furthermore they allow the use of conventionalneurosurgical instruments.

Hall et al. [64, 67] report, that fMRI data is collected before inductionof general anesthesia. The images are viewed during resection. Functional

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MRI demands a good level of cooperation from the patient. We find it contro-versial, that this level of compliance especially for more complex tasks canbe produced routinely immediately before surgery, or even intraoperatively.Our patients undergo fMRI well before the surgery, and the data is integratedinto our navigation system.

MR spectroscopy as well as fMRI requires careful evaluation, which iscurrently difficult to accomplish in real-time intraoperatively. MR angio-graphy with high field MR may prove to be a valuable tool in surgicalremoval of vascular lesions, and for intra-vascular procedures. The abun-dance of image information in high quality is fascinating. It remains an openquestion, however, as to how much time may be spent on intraoperative MRstudies, and what direct impact or benefit they provide for the surgical pro-cedure itself. Furthermore, if this updated information is not integrated intoan interactive visualization tool for neuronavigation, the acquisition lacksapplicability.

Because all the magnets, other than the one installed at our institution(SignaSP), separate imaging and surgical space, either in different rooms, orby moving patient or imaging device, repeated transports result in cumulativetime loss, and computer-assisted navigation is impossible without reregis-tration.

In our opinion most questions that arise during surgery are related todiscerning residual tumor and avoidance of critical brain areas. ConventionalT1-, T2-w and SPGR pulse sequences can adequately address these issues.Undoubtedly, intraoperative functional testing is desirable. Potential benefitsfrom fMRI could be to identify spatial displacement and reactivated areasafter tumor debulking. Nevertheless, direct cortical stimulation yields moreprecise answers with less effort.

The integration of new technologies into clinical routine, such as intraop-erative MRI, has always been cost-and labor-intensive [166]. It remains tobe proven by long tem follow-up studies, if the outcome of the neurosurgi-cal patients is significantly changed. We expect that these techniques, withaccumulating experience, will become standard of care. In the near term, weexpect presurgical planning to improve through more precise definition oftarget tissue, as well as adjacent functional and structural areas, with fMRIand diffusion weighted images [62], and tensor representation of the whitematter tracts. MR imaging will improve through reduced acquisition timesand refinement of imaging sequences for neurosurgical guidance such as“continuous imaging” [167]. MRI monitoring and visualization of minimally

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invasive procedures such as focused ultrasound [168] and interstitial lasertherapy will open new therapeutic avenues.

SUMMARY AND CONCLUSION

We describe the implementation of intraoperative imaging at our institution(GE SignaSP) and its most important neurosurgical applications. Presurgi-cal information and updated data are used for intraoperative neuronavigationwith the 3D Slicer. Intraoperatively serial scanning is done to update the pre-operative information and allows compensation for the inaccuracies inducedby brain shift.

MRI-guided neurosurgical procedures are a collaborative effort, involv-ing neurosurgeons, neuroradiologists, anesthesiologists, MR technologists,nurses, and engineers. This collaboration is essential for further scientificdevelopment [6, 40, 63, 64, 66, 67, 83, 111, 112, 117, 121, 163].

What are the future developments in intraoperative MRI? What are thedesirable features of a prospective intraoperative MRI?

• Full patient-access during the surgical procedure• No need to move either patient or magnet• Highest image quality with reduced acquisition time• Ergonomics that incur no delays for serial or continuous scanning,• Integration of all pre- and intraoperative imaging data for interactive

navigation

An ambitious design might be a high field strength system (1.5 Tesla) asan open design (“tabletop”), with fast acquisitions, and fully integratedcomputer-assisted navigation.

Acknowledgements

We thank the MRT-team for translating research and technology into rou-tine use for patient care and the team of the Surgical Planning Laboratoryspecifically Marianna Jakab and Mark Anderson.

AN was supported by the Deutsche Forschungs Gemeinschaft (NA359/1-1). Further funding: NIH grants P41-RR13218-01, RO1-RR11747-01A, PO1CA67165-03.

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neurosurgical procedures in a 0.5 tesla, open-configuration

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