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Published online before print August 18, 2004, 10.1148/radiol.2331031352
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(Radiology 2004;233:67-78.)
© RSNA, 2004

Neuroradiology

Intraoperative High-Field-Strength MR Imaging: Implementation and Experience in 200 Patients1

Christopher Nimsky, MD, Oliver Ganslandt, MD, Boris von Keller, MD, Johann Romstöck, MD and Rudolf Fahlbusch, MD

1 From the Department of Neurosurgery, University Erlangen-Nürnberg, Schwabachanlage 6, 91054 Erlangen, Germany. Received August 23, 2003; revision requested November 6; final revision received January 26, 2004; accepted February 16. Supported by the Deutsche Forschungsgemeinschaft and the Wilhelm-Sander-Stiftung. Address correspondence to C.N. (e-mail: nimsky@nch.imed.uni-erlangen.de).


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
PURPOSE: To review the initial clinical experience with intraoperative high-field-strength magnetic resonance (MR) imaging of brain lesions in 200 patients.

MATERIALS AND METHODS: Two hundred patients (mean age, 46.1 years; range, 7–84 years), most of whom had glioma or pituitary adenoma, were examined with a 1.5-T MR imager equipped with a rotating operating table and located in a radiofrequency-shielded operating theater. A navigation microscope placed inside the 0.5-mT zone and used in combination with a ceiling-mounted navigation system enabled integrated microscope-based neuronavigation. The extent of resection depicted at intraoperative imaging, the surgical consequences of intraoperative imaging, and the clinical practicability of the operating room setup were analyzed.

RESULTS: Seventy-seven resections with a transsphenoidal approach, 100 craniotomies, and 23 burr-hole procedures were performed. In 55 (27.5%) of 200 patients, intraoperative MR imaging had immediate surgical consequences (eg, extension of resection in 39% of patients with pituitary adenoma or glioma). In 108 patients the navigation system was used, and for 37 of those patients, functional imaging data were integrated into the navigation system. There was nearly no difference in quality between pre- and intraoperative images. Intraoperative workflow with intraoperative patient transport for imaging was straightforward, and imaging in most cases began less than 2 minutes after sterile covering of the surgical site. No complications resulted from high-field-strength MR imaging.

CONCLUSION: The high-field-strength MR imager was successfully adapted for intraoperative use with the integrated neuronavigation system. Intraoperative MR imaging provided valuable information that allowed intraoperative modification of the surgical strategy.

© RSNA, 2004

Index terms: Brain, MR, 18.12141, 18.12143 • Brain neoplasms, 18.36, 18.37, 18.38 • Brain, surgery • Magnetic resonance (MR), guidance


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Intraoperative imaging has attracted increasing interest in recent years. The ability to determine the extent of tumor removal during surgery is advantageous: If the resection appears incomplete, the surgeon can remove the residual tumor during the same procedure. Intraoperative imaging provides immediate quality control during surgery (1). Magnetic resonance (MR) imaging is the method of choice for preoperative diagnosis of brain tumors and epilepsy (2,3). However, the closed-bore design and the strong fringe magnetic fields of the first MR imagers prevented their use in the operating room (4). In the mid-1990s, the development of open MR systems made intraoperative MR imaging possible for the first time. This application was pioneered by Black et al (5).

In 1995, in a first step toward the development of an MR imager dedicated to operating room use, staff from the neurosurgical departments at Erlangen and Heidelberg universities, working in close cooperation with the manufacturer, adapted a low-field-strength MR imager (0.2-T Magnetom Open; Siemens Medical Solutions, Erlangen, Germany), initially designed solely for diagnostic purposes, for surgical use (6,7). Integral to our concept was the possibility of simultaneous intraoperative imaging and neuronavigation. Standard neuronavigation is based on anatomic information only, but we integrated informationfrom preoperative magnetoencephalography and functional MR imaging to localize eloquent brain areas, such as motor and speech areas (8,9). Between March 1996 and July 2001, we performed intraoperative low-field-strength MR imaging in 330 patients (10). Intraoperative MR imaging allowed more complete resections with lower morbidity, while simultaneous use of functional neuronavigation allowed conservation of eloquent brain areas despite extended resections (8,9). The most important uses for intraoperative MR imaging include guidance of resection in patients with glioma (11–15), hormonally inactive pituitary tumor (16,17), or epilepsy (18–20). Intraoperative MR imaging also allows compensation for brain shift (21,22) through updating of information provided by the navigation system with intraoperative imaging data. As demonstrated by other investigators (4,7,11,14), MR imaging is safe and reliable in the surgical environment and is applicable for intraoperative guidance of neurosurgical procedures, although these procedures may have to be adapted somewhat for the MR environment. The development of navigation microscopes that can be used in the fringe magnetic field of the MR imager (23) obviated the cumbersome and time-consuming intraoperative transport of patients and enabled microscope-based navigational support during neurosurgery in the fringe magnetic field.

The image quality generated by various intraoperative low-field-strength MR systems, however, did not compare well with the diagnostic image quality obtained with high-field-strength imagers. In addition, low-field-strength MR imagers could not be used for examinations such as functional or diffusion-weighted imaging or MR spectroscopy. Only two centers had previously attempted to use high-field-strength MR imagers in the operating room. Hall et al (24) adapted a standard 1.5-T imager for the surgical environment. Sutherland et al (25) took an alternative approach and designed a 1.5-T imager specifically for the requirements of the operating room. In their design, the magnet is mounted on the ceiling and moved into the appropriate imaging position. The active shielding of modern high-field-strength magnets results in the close proximity of the 0.5-mT zone to the imager. Thus, our concept of intraoperative MR imaging, in which surgery is performed inside the fringe magnetic field and with microscope-based neuronavigational support, can now be applied with high-field-strength magnets. The purpose of our study was to review the initial clinical experience with intraoperative high-field-strength MR imaging of brain lesions in 200 patients at our institution.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Patient Population
From April 2002, when we began performing intraoperative high-field-strength MR imaging, until July 2003, a total of 200 patients underwent intraoperative MR imaging at our institution. The mean age of these patients was 46.1 years (range, 7–84 years). The patient group consisted of 116 male patients (mean age, 45.0 years; range, 7–77 years) and 84 female patients (mean age, 47.6 years; range, 11–84 years). There was no significant difference in age distribution between the sexes (Mann-Whitney test). Histopathologic examination revealed the lesions to be pituitary adenoma (n = 65); glioma (n = 63); craniopharyngioma (n = 11); meningioma (n = 5); lymphoma (n = 5); dysembryoplastic neuroepithelial tumor (n = 3); cavernoma (n = 3); gliomatosis (n = 3); Rathke cleft cyst (n = 2); chordoma (n = 2); metastasis (n = 2); and carcinoma, cholesterol cyst, abscess, epidermoid, neurocytoma, and primitive neuroectodermal tumor (n = 1 each). In 22 other patients, a tailored temporal lobectomy was performed for treatment of cryptogenic epilepsy. The results of histologic examination revealed gliosis or hippocampal sclerosis in most of these patients. In six other patients with craniopharyngioma and in two other patients with cysts, catheter drainage of the lesion was performed, but no histologic specimen was obtained. The local ethical committee approved intraoperative high-field-strength MR imaging, and signed informed consent was provided by each patient prior to surgery. For children, adult family members provided informed consent.

Operating Room Setup
The 1.5-T imager (Magnetom Sonata Maestro Class; Siemens Medical Solutions) is installed in an operating room with radiofrequency shielding (Fig 1). This high-field-strength imager has a superconductive magnet with a length of 160 cm and an inner bore diameter of 60 cm, as well as a gradient system with a maximum field strength of 40 mT/m (effective, 69 mT/m) and a maximum slew rate of 200 T · m–1 · sec–1 (effective, 346 T · m–1 · sec–1). The rotating surgical table (Trumpf, Saalfeld, Germany) has a tabletop that is specially adapted for MR imaging and that can be locked into various positions. The principal surgical position is at 160°, with the patient’s head at the 0.5-mT line (ie, 4 m from the center of the imager; see Fig 1a). As soon as the rotating mechanism has been locked, the height of the table and the longitudinal and lateral angles can be modified. The table movements are controlled remotely. Only the rotation of the table into and out of the imager is performed manually, for safety reasons.



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  		Figure 1a. (a) Floor plan of operating theater shows two possible operating positions: at 0.5-mT line, with full use of the microscope-based navigation system (A); and in high magnetic field, with use of fully MR-compatible instruments only (B). (b) Panoramic photograph shows operating theater during glioma surgery with the microscope-based navigation system.

 


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  		Figure 1b. (a) Floor plan of operating theater shows two possible operating positions: at 0.5-mT line, with full use of the microscope-based navigation system (A); and in high magnetic field, with use of fully MR-compatible instruments only (B). (b) Panoramic photograph shows operating theater during glioma surgery with the microscope-based navigation system.

 
The ceiling outlet for laminar airflow (Luwa, Frankfurt, Germany) is located above the main operating position (at A in Fig 1a). The laminar airflow outlet is surrounded by a band of fluorescent lamps for optimal illumination. During imaging, the lamps are turned off from the control room. An MR-compatible respirator and anesthesia care monitor (Magnitude; In Vivo Research, Orlando, Fla) are provided (26). The MR-compatible monitor is equipped with a 2.4-GHz wireless data transfer system to enable monitoring from outside the radiofrequency-shielded cabin. The infusion pumps are shielded (MRI-Caddy; MIPM, Mammendorf, Germany) for MR compatibility. The service outlets include sockets connected to different electric circuits so that selected sockets can be switched off from a switchboard in the MR control room to prevent artifacts generated by individual devices. All electric circuits entering the radiofrequency cabin are filtered. Data and video lines of the navigation system and in-room monitors consist of fiberoptic cable.

The microscope (NC4 Multivision; Zeiss, Oberkochen, Germany) is positioned at the left side of the patient’s head, just outside the 0.5-mT line. The electric current to the microscope and to other devices that may interfere with the MR signal is automatically switched off during MR imaging. Two 17-inch flat-screen monitors (AS4431ID; Iyamo, Nagano-Shi, Japan) mounted on a ceiling arm (Ondal, Hünfeld, Germany) are available for viewing the images from the microscope and the MR console, as well as various software applications. The 0.5-mT and 20-mT lines are marked on the floor. The 20-mT line also is marked with a raised stainless steel strip as a physical threshold. All equipment that is not completely MR compatible, such as the navigation microscope and the height-adjustable surgeon’s chair, is mechanically secured to the wall of the radiofrequency-shielded room. The instrument table and the various rotating stools (Trumpf) are fully MR compatible.

The procedures for emergency magnet quenching and for monitoring of oxygen levels in the operating room are the same as those in standard clinical MR imaging installations.

Neurosurgical guidance is provided by a navigation system (VectorVision cranial; BrainLAB, Heimstetten, Germany). A fiberoptic connection ensures MR-compatible integration of the navigation system with other instruments in the operating room. The camera used to monitor the positions of the microscope, and the touch-sensitive screen used to operate the navigation system, are ceiling mounted.

Preoperative MR Imaging
A 1.0-mm isotropic three-dimensional MR image data set was obtained with a magnetization-prepared rapid-acquisition gradient-echo sequence (repetition time msec/echo time msec, 2020/4.38; field of view, 250 mm; imaging time, 8 minutes 39 seconds) prior to surgery, for use as a navigational reference data set into which functional imaging data could be integrated. To facilitate image data registration, between five and seven skin-adhesive fiducial marks were placed in a scattered pattern on the head surface prior to imaging. The position of the fiducial marks was defined in the three-dimensional data set and registered with a pointer. Functional data from magnetoencephalography and functional MR imaging performed preoperatively were integrated with the three-dimensional data set (8,9). For estimating the accuracy of navigation, the mean registration error was documented by placing a navigation pointer in the center of an additional fiducial mark that was not used for registration and measuring the distance between the pointer position and the center of the fiducial mark on the navigation system screen. Repeated visual checks of anatomic landmarks were performed to ensure continued overall accuracy of the image registration. If intraoperative images depicted residual tumor that could be resected, the intraoperative MR imaging data were used to update the navigation information. After rigid registration of preoperative and intraoperative images, initially accomplished with manual alignment of matching coordinates and subsequently optimized by using software (ImageFusion; BrainLAB) based on pyramidal mutual information about signal intensity, the initial registration file (ie, the navigation reference data obtained with the initial registration of preoperative MR imaging and functional data with the microscope-based navigation information) was restored so that no repeated image registration procedure was needed. A prerequisite was that there be no movement of the patient’s head in relation to the coordinate system between navigation data registration and intraoperative imaging.

Intraoperative MR Imaging
An MR-compatible four-point head holder made of glass fiber–reinforced plastic was integrated into a circular polarized head coil and used for head fixation during craniotomies and burr-hole procedures. The upper part of the head coil could be sterilized by using plasma sterilization. Sterile adapters were placed on the lower part of the head coil to allow sterile draping. In transsphenoidal surgery, which does not require head fixation, imaging was performed by using a flexible U-shaped coil adapted to the head.

After the patient was placed in the bore of the imager, unneeded electric circuits were switched off, including those supplying current to the fluorescent lamps, the navigation microscope, and the part of the navigation system located in the radiofrequency cabin. Then imaging was performed, beginning with a localizer sequence (20/50; field of view, 280 mm; imaging time, 9 seconds). For transsphenoidal surgery, a T2-weighted half-Fourier rapid acquisition with relaxation enhancement sequence (1000/89; section thickness, 5 mm; field of view, 230 mm; five signals acquired; imaging time, 25 seconds) was applied in the coronal and sagittal directions to obtain a quick overview. Afterward, a T1-weighted spin-echo pulse sequence (450/12; section thickness, 3 mm; field of view, 270 mm; four signals acquired; imaging time, 4 minutes 57 seconds) was applied in the same planes. In addition, a high-spatial-resolution (in-plane resolution, 0.6 x 0.4 mm) T2-weighted turbo spin-echo sequence (4000/97; section thickness, 3 mm; field of view, 230 mm; three signals acquired; imaging time, 6 minutes 6 seconds) was applied. For glioma surgery, the imaging protocol included the following sequences applied in the transverse plane: T2-weighted turbo spin echo (6490/98; section thickness, 4 mm; field of view, 230 mm; three signals acquired; imaging time, 5 minutes 39 seconds), fluid-attenuated inversion recovery (10 000/103; section thickness, 4 mm; field of view, 230 mm; one signal acquired; imaging time, 6 minutes 2 seconds), T1-weighted spin echo (525/17; section thickness, 4 mm; field of view, 230 mm; two signals acquired; imaging time, 3 minutes 59 seconds), and fluid-suppressed echo planar (9000/85; section thickness, 5 mm; field of view, 230 mm; one signal acquired; imaging time, 1 minute 2 seconds). If the tumor was contrast material enhanced on preoperative MR images, the transverse T1-weighted spin-echo sequence was repeated after intravenous administration of 0.2 mL of gadopentetate dimeglumine (Magnevist; Schering, Berlin, Germany) per kilogram of body weight, the same contrast material and dose administered at preoperative MR imaging. Afterward, the 1.0-mm isotropic three-dimensional data set obtained with the magnetization-prepared rapid-acquisition gradient-echo sequence for navigational reference, as described earlier, was measured. This sequence allowed free reformatting of images and intraoperative updating of information in the navigation system (22). In patients undergoing epilepsy surgery or other procedures (eg, biopsy), a reduced MR imaging protocol was applied. If findings at intraoperative imaging led to further resection, imaging was repeated after completion of the tumor resection and prior to the closure of the wound. Contrast medium administration was not repeated.

Data Analysis
The clinical practicability of the setup was documented for each procedure, and potential technical problems of intraoperative imaging and intraoperative workflow, as well as integration of the navigation system, were recorded. Imaging quality was assessed with a visual comparison between corresponding pre- and intraoperative image data sets, with special attention given to intraoperative imaging artifacts. Image interpretation and analysis were performed by two authors (C.N., O.G.) in consensus. All procedures were analyzed with respect to any modification of the surgical strategy, such as an extension of the resection, as a result of intraoperative imaging. The patients with pituitary adenomas, which were resected with a transsphenoidal approach, were grouped according to whether tumor removal was intended to be complete or incomplete. Resection completeness was analyzed for the group with intended complete removal. The patients who underwent glioma resection were similarly grouped. In addition to resection completeness and extension of the resection, the effect of intraoperative MR imaging on reduction of the residual tumor volume was evaluated. In the glioma patients with an extension of resection because of findings at intraoperative MR imaging, the residual tumor volume detected on the first intraoperative MR images was compared with the residual volume after further resection. Volume was calculated with manual segmentation of the tumor outline on the registered T1- and T2-weighted images by using the navigation software. All procedures were monitored for complications related directly to imaging. Furthermore, a follow-up neurologic evaluation was performed in all patients, and patient records were reviewed for delayed postoperative complications such as wound infections.

Statistical Analysis
Data were analyzed by using statistical software (SPSS, version 11.5; SPSS, Chicago, Ill). Differences between groups were analyzed by using the nonparametric Mann-Whitney test. P < .05 was considered to represent a statistically significant difference.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
Intraoperative MR imaging was performed during 77 transsphenoidal procedures (in lesions that included 62 pituitary adenomas and eight craniopharyngiomas), 100 craniotomies (in lesions that included 51 gliomas and 22 cases of gliosis or hippocampal sclerosis in epilepsy), and 23 burr-hole procedures (in lesions that included 12 gliomas and six craniopharyngioma cyst punctures).

Clinical Practicability
As a general rule, intraoperative imaging was begun less than 2 minutes after the neurosurgeon decided to use it. With the anesthesia catheters and monitoring cables to and from the patient passing through the center of rotation of the surgical–MR imaging table, there were no delays in regard to anesthesia. The flexibility of the rotatable and adjustable surgical–MR imaging table was similar to that of a standard surgical table. The head holder integrated into the head coil allowed variable access with the patient either supine or prone. (Lateral placement of the patient was possible only with a slender body habitus because the inner bore of the imager is only 60 cm in diameter.) With the patient supine and the shoulder elevated, the head could be positioned horizontally at a 90° angle, if desired. Access to the craniotomy site, however, was limited to a certain extent by the coil adapters. Further modifications of this prototype head holder are needed.

The integrated microscope-based neuronavigation system was used without problems (Table 1). Preparation time for navigation, including data transfer, segmentation, definition of reference points, and registration, in most cases was 10 minutes or less. Location in the vicinity of the fringe magnetic field did not affect neuronavigation system operation. The mean registration error per case ranged from 0.3 to 2.9 mm (mean for all cases, 1.3 mm; standard deviation, 0.9 mm). Intraoperative updating of the neuronavigation system enabled the surgeon to identify areas of residual tumor for removal with reliable accuracy in all cases.


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  		TABLE 1. Application of Navigation System for Neurosurgical Procedures

 
Intraoperative Imaging
Intraoperative MR imaging was technically feasible in all cases. In only one case did we encounter technical difficulties. During one of the first transsphenoidal procedures, a coil cable broke during use of the flexible coil and had to be replaced. No artifacts caused by the operating room environment were observed. The ability to turn off the fluorescent lamps and specific power outlets from the MR control room proved very helpful. The intraoperative image quality obtained with the high-field-strength imager was clearly superior to that achieved with low-field-strength MR systems. Hardly any difference could be observed between the quality of preoperative and intraoperative images in all 200 cases. In addition, the high-field-strength imager allows shorter examination times, or the application of further sequences in the same examination time. For example, when T2-weighted half-Fourier rapid acquisition with relaxation enhancement is used to verify the completeness of resection of pituitary tumors, the extent of resection often can be determined within a few seconds (Fig 2). As a consequence, our intraoperative imaging protocol in patients with pituitary tumors starts with a time-saving half-Fourier rapid acquisition with relaxation enhancement sequence, which allows immediate resumption of surgery if a tumor remnant is depicted.



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  		Figure 2. MR images in a 29-year-old female patient in less than 1/2 minute with T2-weighted half-Fourier rapid acquisition with relaxation enhancement (1000/89). Preoperative images show sagittal (A) and coronal (B) views of intra- and suprasellar pituitary adenoma (arrows). Intraoperative images show sagittal (C) and coronal (D) views of extent of resection.

 
Consequences of Intraoperative Imaging
Intraoperative MR imaging resulted in a modification of surgical strategy (ie, an extension of the resection or a correction of the placement of a biopsy needle or catheter) in 55 (27.5%) of 200 cases (Table 2).


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  		TABLE 2. Modification of Surgical Strategy after Intraoperative MR Imaging

 
In transsphenoidal surgery for pituitary adenoma, evaluation of suprasellar tumor removal was possible in all cases; in the majority of patients, even the structures of the cavernous sinus could be evaluated reliably, as well. In the 14 patients with adenoma in which partial resection was planned, intraoperative imaging delineated the exact extent of resection and the location of the remaining tumor tissue (eg, in the parasellar structures). Among the 48 patients with pituitary adenomas that had distinct suprasellar extension and that appeared to be resectable, findings at intraoperative MR imaging led to a repeated inspection of the surgical site in 29 (60%). Repeated surgical inspection in 19 of the 29 patients revealed residual tumor tissue that could be at least partly removed. In 15 of these patients, the tumor was resected in its entirety. The use of this intraoperative imaging technique thus resulted in an increase in the rate of complete tumor removal from 56.2% (27 of 48 lesions) to 87.5% (42 of 48 lesions) (Fig 3). In the other 10 patients, repeated inspection of the surgical site was performed to identify the nature of intra- and parasellar findings on the intraoperative T1-weighted images that were suspicious for residual adenoma. The findings consisted of fibrin glue, blood, and a suprasellar fold. Because T2-weighted imaging allowed better delineation of pituitary adenoma, our standard protocol for intraoperative imaging in transsphenoidal surgery was changed from T1- to T2-weighted imaging.



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  		Figure 3. Sagittal MR images in a 56-year-old woman with pituitary adenoma. A-C, T1-weighted (450/12) images. D, E, T2-weighted (4000/97) images. A, Preoperative image shows large intra- and suprasellar pituitary adenoma (arrow). B, Intraoperative image acquired after initial resection shows small tumor remnant in posterior portion of the sella (arrow), which was removed with further resection. C, Postoperative image shows no evidence of tumor after further resection. Intraoperative (D) and postoperative (E) high-spatial-resolution T2-weighted images provide, respectively, clearer delineation of tumor remnant (arrow) and of its absence after resection.

 
Among patients who underwent resection of glioma, intraoperative imaging revealed incomplete tumor removal initially in 39 (80%) of 49 (Table 3). In 20 patients with incomplete tumor removal, further resection was abandoned despite obvious residual tumor on intraoperative images, because of the infiltration of eloquent brain cortex or critical anatomic structures. This group included two patients with World Health Organization (WHO) grade II tumors, five with WHO grade III tumors, and 13 with WHO grade IV tumors. In one of the 19 patients who underwent further resection, intraoperative MR imaging was performed three times; in the other patients, it was performed twice. As a result, gross total removal was achieved in 17 (35%) of 49 patients (Table 3; Figs 4, 5). Of the 17 patients in whom resection was complete, seven (41%) underwent further resection after intraoperative MR imaging. The results of volumetric assessment of glioma during resection showed a significant reduction in residual tumor volume as a result of extended resection after intraoperative MR imaging: Residual tumor volume decreased from 26.5% to 11.6% in patients with intended partial resection (Table 4).


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  		TABLE 3. Intraoperative MR Imaging Findings during Glioma Resection

 


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  		Figure 4. Transverse MR images in a 45-year-old male patient with left-sided glioblastoma. Preoperative views obtained with T1-weighted (A; 525/17), T2-weighted (B; 6490/98), and fluid-attenuated inversion-recovery (C; 10 000/103) sequences show tumor with contrast material-enhanced areas (arrows). D-F, Corresponding intraoperative images obtained with the same series of pulse sequences as in A-C show that contrast-enhanced areas of tumor have been completely removed.

 


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  		Figure 5. Transverse T2-weighted (6490/98) MR images in a 20-year-old woman with right-sided precentral astrocytoma of WHO grade II. A, Preoperative tumor. B, Intraoperative image shows complete tumor removal.

 

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  		TABLE 4. Comparison of Residual Tumor Volumes in Patients Who Underwent Extended Resection for Glioma because of Findings at Intraoperative MR Imaging

 
In surgery for nonlesional temporal lobe epilepsy, intraoperative MR imaging allowed a clear delineation of the extent of temporal lobectomy. Furthermore, the appropriate placement of subdural and hippocampal strip electrodes could be determined with intraoperative imaging (Fig 6). Figure 7 depicts a ventricular tumor, in which intraoperative imaging led to further resection. In all burr-hole procedures (n = 23), intraoperative imaging enabled the localization of the catheter or of the biopsy site. In two of the six patients with large cystic craniopharyngiomas, intraoperative MR imaging revealed that the catheter had not penetrated the cyst wall and that no drainage of the cyst to the lateral ventricle had been established. A second puncture was successful, as shown at repeated intraoperative imaging. For all 15 burr-hole biopsies, a histologic diagnosis was obtained. Intraoperative MR imaging allowed the surgeon to determine whether the needle was appropriately placed to obtain a histologic specimen at the preplanned location; in one patient, a correction of the biopsy needle path resulted.



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  		Figure 6. T2-weighted (6490/98) MR images in a 30-year-old woman with pharmacoresistant epilepsy caused by temporal lobe abnormality. A-C, Transverse views. D-F, coronal views. A, D, Preoperative images. B, E, Intraoperative images of corresponding sections after craniotomy and placement of subdural strip electrodes (arrow in B, small arrows in E) and hippocampal electrode (large arrow in E). C, F, Intraoperative images of same sections after tailored right temporal lobectomy.

 


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  		Figure 7. Coronal T2-weighted (6490/98) MR images in a 37-year-old man with ventricular neurocytoma. A, Preoperative image shows tumor location and indicates transcallosal approach. B, Intraoperative image shows tumor remnants (arrows). C, Intraoperative image obtained after further resection confirms complete removal of tumor.

 
Complications
No adverse events occurred because of the high magnetic field strength. Although standard microinstruments were used at the 0.5-mT line, there were no ferromagnetic accidents. Anesthesia monitoring was uneventful. Four patients developed wound infections in the early postoperative course and underwent local revision. In this group, one patient underwent revision for each of the following initial procedures: glioma resection, glioma biopsy, nonlesional epilepsy surgery, and craniopharyngioma cyst puncture. One patient who underwent surgical resection for a large pituitary adenoma died of pulmonary embolism on the second postoperative day. Intraoperative intracerebral hemorrhage could be excluded in all patients undergoing burr-hole procedure or craniotomy. Prolonged postoperative-onset neurologic deficits were observed in only two patients (4% of the glioma patients who underwent resection), who had tumors infiltrating the motor cortex. In both patients, postoperative hemiparesis resolved after 3 months. In another patient, who underwent removal of a tumor adjacent to language-eloquent areas, mild postoperative dysphasia occurred that lasted 12 hours before resolving completely.


   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
In the mid-1990s, a limited number of hospitals worldwide were attempting to generate MR images of the brain during surgery (5–7). The first imagers used for this purpose were based on magnets with field strengths of 0.5 T or less (10,13–15,27). In terms of the diagnostic quality of images, however, intraoperative low-field-strength MR imaging systems cannot compete with the high-field-strength imagers used for routine neuroradiologic diagnosis. So far, two different concepts for intraoperative high-field-strength imaging have been realized (24,25). As with the intraoperative low-field-strength imagers, there are basically two possibilities: adaptation of a standard diagnostic imager for use in the operating room (24), or design of an imager specifically for the requirements of an operating room (25). Our approach—the adaptation of a rotating surgical table for use with a standard imager—allowed us to combine intraoperative high-field-strength MR imaging with microscope-based neuronavigation.

Clinical Practicability
From April 2002 to July 2003, we examined 200 patients with a 1.5-T MR imager. We did not encounter an increase in problems with artifacts caused by the high magnetic field strength, but, rather, fewer artifacts than with the previous system (10). This decrease in artifacts may be mainly due to an improved operating room design, which provides greater flexibility for eliminating artifacts caused by devices in the operating room, as well as an improved coil design for intraoperative imaging. (The coil used with the initial low-field-strength imaging system was a source of major problems.) Intraoperative high-field-strength MR imaging is safe and reliable: No adverse events occurred because of the high magnetic field strength, and, although standard surgical instruments were used in the 0.5-mT zone, there were no ferromagnetic accidents. With regard to complications due to intraoperative imaging, the integration of functional data into the anatomic navigational data sets is an important addition to intraoperative MR imaging, since it permits the avoidance of postoperative neurologic deficits due to resection. We observed prolonged new (postoperative) neurologic deficits in only 4% of patients who underwent surgical resection for glioma. The rate of wound infections, at 2%, is within the range for our regular operating theaters.

With respect to the practicability of intraoperative MR imaging, we found a distinct improvement over our previous designs (6,10,23). The time needed to prepare for intraoperative imaging was reduced. In addition, the use of the integrated microscope-based neuronavigation system was straightforward. Patient positioning was still limited to a certain extent; procedures in the sitting position were not possible, which is a drawback for posterior fossa surgery. Despite the clearly facilitated intraoperative patient transport with the adapted rotating table, intraoperative patient transport and imaging, of course, interrupted the surgical workflow. However, there is as yet no alternative concept for intraoperative high-field-strength MR imaging without transport of either the patient or the imager. In the future, short magnets with a large bore may allow the use of high-field-strength MR imaging for monitoring in open-cranium surgery without the need for any intraoperative transport.

Acquisition of the three-dimensional data set for neuronavigation prior to surgery but after induction of anesthesia and head fixation (to exclude any shifting of registration markers) was a prerequisite for a low registration error. The navigation system, updated with intraoperative image data in more than one-fourth of all patients for whom navigation was used, allowed reliable intraoperative localization of residual tumor. Compared with previous methods that necessitated time-consuming intraoperative reregistration (21,22), the procedure that we used, which included the restoration of registration data, facilitated updating.

We expect that the possibility of automatic registration of images, which is currently under development, will result not only in further time saving but also in improved accuracy. Other improvements will relate to head fixation during craniotomy and to the use of different coils to improve ergonomics for the surgeon. The results of our current study clearly confirm distinct improvements in intraoperative image quality with our new system, compared with our previous 0.2-T system (10). The results of our comparison of pre- and intraoperative images indicate no substantial limitations. We think that the clear improvement in image quality may increase the reliability of information regarding the extent of resection (ie, the presence and exact location of residual tumor tissue).

Major Indications for Intraoperative MR Imaging
In 27.5% of patients, findings at intraoperative MR imaging led to modification of the surgical procedure (eg, further tumor resection or correction of catheter position). Among patients who had either of the two major indications for intraoperative MR imaging, transsphenoidal pituitary adenoma or glioma, the proportion was even higher (39% for both groups). A comparison of these rates with those from our previous low-field-strength experience (34% for patients with adenoma and 26% for those with glioma) (17,28) supports the impression that the clear improvement of image quality with the high-field-strength MR system also may result in increased rates of resection extension.

In transsphenoidal pituitary adenoma surgery, reliable imaging of suprasellar tumor removal was possible in all cases. In contrast to low-field-strength systems, with which the evaluation of the intrasellar space was rarely possible (17), high-field-strength imaging enables the reliable evaluation also of cavernous sinus structures in most patients. Intraoperative imaging resulted in an increase from 56.2% to 87.5% in the rate of complete tumor removal in patients in whom complete removal initially seemed possible via the transsphenoidal approach. Early (ie, intraoperative) visualization of tumor remnants that are not removable allows immediate planning of further postoperative treatment options, such as surveillance, radiation therapy, or transcranial surgery. Without intraoperative imaging, such planning would not be possible until 2 to 3 months after surgery, because artifacts at early postoperative imaging after transsphenoidal surgery prevent reliable visual evaluation (17,29).

For gliomas, at present the standard treatment is maximum safe resection, and, for high-grade gliomas, subsequent adjuvant treatment such as radiation therapy and/or chemotherapy (30–32). Additional further resection due to findings at intraoperative MR imaging significantly reduced the percentage of the final tumor volume, compared with tumor volume at initial intraoperative MR imaging. In low-grade gliomas, there is little question that complete removal of all tumor tissue is an ideal treatment that may lead to cure. If residual tumor tissue is present, however, it eventually degenerates into a glioblastoma multiforme, with resultant limitation of patient life expectancy (1). Aggressive resection even in high-grade gliomas is associated with longer survival of patients, according to several reports (33–36).

Intraoperative MR imaging proved helpful in a variety of other indications, as well. It provided immediate intraoperative quality control with respect not only to the extent of resection but also to the avoidance of complications. Exclusion of intracerebral hemorrhage and confirmation of the biopsy site were major advantages with the use of intraoperative imaging in burr-hole biopsies. Intraoperative imaging proved helpful also in epilepsy surgery (18–20) and craniopharyngioma management. With regard to craniopharyngioma removal, it is too early to decide whether high-field-strength MR imaging is more sensitive than low-field-strength MR imaging in depicting small tumor islets that may lead to craniopharyngioma recurrence (37).

Future Developments
MR spectroscopy and diffusion-weighted imaging have been used recently for diagnosis and treatment planning in patients with glioma (38–41). These modalities can provide detailed information about diffuse tumor borders. The integration of such information into the neuronavigation system allows the correlation of spatial data with histopathologic findings. Functional data from magnetoencephalography and functional MR imaging only localize function at the brain surface; however, neurologic deficits also may be caused by damage to deeper structures, such as the brain pathways, during resection. Diffusion-tensor imaging can be used not only to delineate tumor borders but also to display the course of white-matter tracts, such as the pyramidal tract (42–44). Registration of these data with the navigational data set (45) will facilitate the intraoperative preservation of these structures, if the intraoperative changes of the brain anatomy, known as brain shift, are taken into account (22). Mathematic models that describe brain shift by using finite elements will help to localize preoperative functional data in intraoperative data sets (46,47). The reliability of intraoperative functional imaging (eg, intraoperative functional MR imaging) during open-skull surgery is under investigation.

Aside from the indications currently defined for use of intraoperative low-field-strength MR imaging, intraoperative high-field-strength MR imaging may also have important uses—for example, in vascular surgery. It is not enough that MR angiography depict the complete clipping of an aneurysm; diffusion-weighted imaging enables the intraoperative visualization of blood supply to the brain and, thus, can help detect or prevent a reduction in perfusion (48). Intraoperative MR imaging may also prove useful in spinal surgeries, such as the resection of complex intramedullary tumors or drainage of syringomyelias. The integration of intraoperative MR imaging with robot-assisted surgery is another potential future development (49).

At present, intraoperative high-field-strength MR imaging with integrated microscope-based neuronavigation is one of the most highly developed techniques for obtaining reliable intraoperative verification of the immediate effects of a surgical procedure so that appropriate decisions (eg, to extend a resection) can be made and implemented during the same procedure.

It was beyond the scope of this study to investigate the long-term effects of intraoperative MR imaging—for example, whether an extended resection in pituitary adenomas or gliomas results in lower recurrence rates, prolonged delay before recurrence, or even prolonged survival. Although some patients clearly have benefitted from the technique applied, a randomized prospective study in which outcomes with and without intraoperative MR imaging are compared nevertheless would be desirable. In the meantime, however, we doubt that patients will be willing to undergo surgery without intraoperative imaging, if the technology is available to them at a certain center. Furthermore, we must emphasize that, especially for the treatment of gliomas, critical advances are expected, particularly in molecular biology. Careful consideration of the indications for use of this complex and expensive technology, accurate cost-benefit analyses (1,50), and investigations into the long-term effects of intraoperative MR imaging, especially with respect to tumor recurrence and, in gliomas, time to progression, as well as life expectancy (15,31), will be essential in the near future.


   ACKNOWLEDGMENTS
 
We appreciate the special efforts of Erich Reinhardt, PhD, chief executive officer of Siemens Medical Solutions, which enabled us to realize the installation as early as possible. We also acknowledge the continued support of Edgar Müller, PhD, and Theodor Vetter, PhD, both also at Siemens Medical Solutions. We thank Stefan Vilsmeier, Niels Ehrke, and Akos Dombay at BrainLAB for their active support in the integration of the navigation system. At our institution, we thank Torsten Uhlemann for valuable assistance with the construction of the new operating theater and Stefanie Kreckel for helpful technical assistance. We also thank the other staff members, neurosurgeons, and radiologists who have contributed to our intraoperative MR imaging capability.


   FOOTNOTES
 
Abbreviation: WHO = World Health Organization

Authors stated no financial relationship to disclose.

Author contributions: Guarantors of integrity of entire study, C.N., R.F.; study concepts, C.N., R.F.; study design, C.N., O.G., J.R.; literature research, C.N., O.G., B.v.K.; clinical studies, C.N., O.G., J.R., R.F.; data acquisition, C.N., O.G., B.v.K.; data analysis/interpretation, C.N., O.G.; statistical analysis, C.N., B.v.K.; manuscript preparation and editing, C.N.; manuscript revision/review, C.N., O.G., R.F.; manuscript definition of intellectual content and final version approval, all authors


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
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