J Neurosurg 121:810–817, 2014 ©AANS, 2014

Awake craniotomy for in a high-field intraoperative magnetic resonance imaging suite: analysis of 42 cases

Clinical article

Marcos V. C. Maldaun, M.D.,1 Shumaila N. Khawja, M.D.,1 Nicholas B. Levine, M.D.,1 Ganesh Rao, M.D.,1 Frederick F. Lang, M.D.,1 Jeffrey S. Weinberg, M.D.,1 Sudhakar Tummala, M.D.,2 Charles E. Cowles, M.D., M.B.A.,3 David Ferson, M.D.,3 Anh-Thuy Nguyen, M.D.,3 Raymond Sawaya, M.D.,1 Dima Suki, Ph.D.,1 and Sujit S. Prabhu, M.D., F.R.C.S.1 Departments of 1Neurosurgery, 2Neuro-Oncology, and 3Anesthesiology, The University of Texas MD Anderson Cancer Center, Houston, Texas

Object. The object of this study was to describe the experience of combining awake craniotomy techniques with high-field (1.5 T) intraoperative MRI (iMRI) for tumors adjacent to eloquent cortex. Methods. From a prospective database the authors obtained and evaluated the records of all patients who had undergone awake craniotomy procedures with cortical and subcortical mapping in the iMRI suite. The integration of these two modalities was assessed with respect to safety, operative times, workflow, extent of resection (EOR), and neurological outcome. Results. Between February 2010 and December 2011, 42 awake craniotomy procedures using iMRI were per- formed in 41 patients for the removal of intraaxial tumors. There were 31 left-sided and 11 right-sided tumors. In half of the cases (21 [50%] of 42), the patient was kept awake for both motor and speech mapping. The mean duration of surgery overall was 7.3 hours (range 4.0–13.9 hours). The median EOR overall was 90%, and gross-total resection (EOR ≥ 95%) was achieved in 17 cases (40.5%). After viewing the first MR images after initial resection, further resection was performed in 17 cases (40.5%); the mean EOR in these cases increased from 56% to 67% after further resection. No deficits were observed preoperatively in 33 cases (78.5%), and worsening neurological deficits were noted immediately after surgery in 11 cases (26.2%). At 1 month after surgery, however, worsened neurological func- tion was observed in only 1 case (2.3%). Conclusions. There was a learning curve with regard to patient positioning and setup times, although it did not adversely affect patient outcomes. Awake craniotomy can be safely performed in a high-field (1.5 T) iMRI suite to maximize tumor resection in eloquent brain areas with an acceptable morbidity profile at 1 month. (http://thejns.org/doi/abs/10.3171/2014.6.JNS132285)

Key Words • awake craniotomy • cortical mapping • surgery • iMRI • EOR • oncology

he goal of glioma surgery is maximal safe resec- ing or improving neurological function while operat- tion of tumors. A number of studies, although ing in eloquent brain areas requires an understanding of not randomized Class I studies, have shown that both the anatomical and functional limits of the tissues Tmaximizing the extent of resection (EOR) improves pro- involved. Awake craniotomy with electrophysiological gression-free survival as well as overall survival in both monitoring is currently the gold standard to achieve the high- and low-grade gliomas.1,7,10,17 The challenges for functional limits of resection.8,16,20 Intraoperative MRI neurosurgeons in achieving a maximal safe resection are (iMRI) has been successfully used to maximize the resec- significant, as a large number of gliomas appear either tion of gliomas and improve patient survival.4,19 By com- in and or adjacent to eloquent brain regions. Maintain- pensating for brain shift during surgery, iMRI improves accurate anatomical visualization of residual tumor and functional tissue. Besides tumor resection, awake crani- Abbreviations used in this paper: DTI = diffusion tensor imag- otomy procedures in the iMRI suite also provide chal- ing; DWI = diffusion-weighted imaging; EOR = extent of resec- tion; fMRI = functional MRI; GTR = gross-total resection; iMRI = This article contains some figures that are displayed in color intraoperative MRI; LMA = laryngeal mask airway; OR = operating online­ but in black-and-white in the print edition. room; PR = partial resection; STR = subtotal resection.

810 J Neurosurg / Volume 121 / October 2014 Awake craniotomy in intraoperative MRI lenges, especially as relates to patient positioning and of famotidine, and 10 mg of metoclopramide, all given anesthesia techniques. A few studies have described the intravenously. To induce anesthesia, we intravenously ad- awake craniotomy procedure in a high-field (1.5 T) iMRI minister 50–100 mg of propofol plus 0.1–0.2 μg/kg/min suite.3,11–13,24 Our group has previously demonstrated the of remifentanil with or without 50 mg of rocuronium. An safety of combining multimodality electrophysiological LMA is then inserted, and the patient is gently turned to monitoring with high-field (1.5 T) iMRI for the resection the appropriate position, usually the right or left lateral of gliomas in eloquent brain areas.5 Here we report on a position. In some instances, especially for frontal tumors, consecutive series of 42 cases (41 patients) treated with a supine position with the head turned is used. The pa- awake craniotomy in the high-field iMRI suite and dis- tient is placed comfortably with adequate padding of any cuss our experience in this patient population. bony prominences against the mattress of the operating table. After this, approximately 40 ml of 0.5% ropiva- caine with 1:200,000 epinephrine is used to block sen- Methods sation in the scalp and forehead. The cutaneous nerves Patient Selection supplying the scalp that are regionally blocked include the greater occipital, lesser occipital, auriculotemporal, Clinical information was obtained from the Department zygomaticotemporal, and supraorbital nerves. The head of Clinical and Imaging Database and The is immobilized using a 3- to 5-point fixation device, and University of Texas MD Anderson Cancer Center Tumor after proper ventilation and positioning, the patient un- Registry. These data were searched for all awake craniot- dergoes preoperative scanning. omy procedures performed for the removal of intraaxial During the asleep portion of the operation, anesthesia tumors near and/or within eloquent cortices using iMRI is maintained with sevoflurane or isoflurane plus remi- between February 2010 and December 2011. Patients had fentanil (0.05–0.2 μg/kg/min). Ropivacaine 0.5% with been selected for the procedure since their tumors had epinephrine is also used along the skin incision. After the a close anatomical relationship to eloquent brain regions craniotomy flap is opened, the dura mater is blocked with according to preoperative MRI. These regions included a 1:1 mixture of 1% lidocaine and 0.25% . receptive and expressive speech areas in the dominant Once the dura is opened, the patient is gradually awak- hemisphere and motor or sensory cortex in either hemi- ened. At this point, all medications are stopped, usually sphere. The institutional review board at the MD Ander- with a 30-minute lead time requested. If the patient be- son Cancer Center approved and reviewed this study. comes uncomfortable during the resection, remifentanil The mean preoperative tumor volume was measured (0.02 μg/kg/min) is restarted. Once the awake testing in all patients using postcontrast T1-weighted MR images portion is complete along with resection of the tumor, the obtained before and after resection. In nonenhancing tu- patients requiring reintubation with the LMA are re-se- mor, T2-weighted images were used for volume determi- dated with dexmedetomidine (0.5–0.7 μg/kg/hr), propo- nation. Postoperative MRI was performed in all patients fol (25–50 μg/kg/min), and remifentanil (0.02–0.05 μg/ within 48 hours of the craniotomy procedure. A computer- kg/min) until the end of the procedure. For some patients, ized volumetric analysis technique, as described by Shi et 21 dexmedetomidine is given as an alternative after func- al., was applied using Vitrea software (Vital Images Inc.). tional testing and during closure, and no LMA is used for Before each awake craniotomy procedure, patients under- these cases. went a complete neurological examination performed by The anesthetic technique used in the iMRI suite the attending physician. Language function was also as- is the same as that used in the regular operating room sessed in a detailed examination by neuropsychologists, (OR) with slight modifications. Sevoflurane or isoflurane including object naming and recall, counting, language flu- is used instead of desflurane (desflurane vaporizer is not ency and comprehension, reading, and writing. compatible with MRI), and the Classic or Supreme LMA, instead of the Proseal LMA, is used because of the lat- Anesthesia Technique ter’s metal reinforced shaft. Extra medications are used The first step in planning an awake craniotomy in the for priming since longer intravenous and infusion lines iMRI suite is preoperative assessment and interview of are required. Patients take longer to awaken since sevo- the patient, which are performed by the surgeon and an- flurane or isoflurane is used, and the duration of a case is esthesiologist. In addition, the surgical plan as well as ex- longer because of added scan times. plicit details of what to expect and what will be required The iMRI unit’s design and the need for equipment of the patient is explained to him or her. A specific his- in the OR to be MRI compatible are unique challenges. tory regarding claustrophobia, anxiety, obstructive sleep Some of these challenges include OR setup rearrange- apnea, and pain conditions involving the body contralat- ments; a decrease in immediate accessibility to all medi- eral to the side of surgery is solicited. The asleep-awake- cations, equipment, and extra personnel; occasionally the asleep technique using the laryngeal mask airway (LMA) less-than-ideal positioning of the patient on the MRI ta- in combination with a scalp block is primarily used for ble; and an increase in patient discomfort. The equipment awake craniotomies in the iMRI suite at our institution. and booms in the iMRI suite are rearranged for awake In our series, the asleep-awake-asleep anesthetic craniotomy cases. Figure 1 shows the OR setup for a left- technique was adopted as described by Huncke et al.6 Af- sided awake craniotomy procedure with the head of the ter MRI-compatible patient monitors (Invivo) are applied, table outside the 5-gauss line. Power is isolated to certain the patients routinely receive 4 mg of ondansetron, 20 mg outlets during the scan mode, which may impair the op-

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geon via a microphone that is placed beside him or her. The patient is then asked to perform verbal and visual tasks to facilitate identification of speech areas during stimulation. Any speech hesitation, dysnomia, and speech arrest are noted. An Ojemann stimulator (Radionics Inc.) with 5-mm spacing between the electrodes is used. It is a constant-current generator that produces a train of square-wave biphasic pulses of 1-msec phase duration at a frequency of 60 Hz. For localization of the primary language and motor cortices, stimulus is applied in incre- ments of 1 mA, starting at 0.5 mA; the rolandic cortex is also identified by somatosensory evoked potentials to identify phase reversals and latency shift. The duration of the stimulus on the brain surface is 2 seconds each time. A cortical area is considered eloquent if a motor response or twitch is generated or language errors are made con- Fig. 1. The OR setup for a left-sided awake craniotomy procedure sistently on at least two separate trials. No cortical site with the head of the table outside the 5-gauss line (yellow). Anesthetic is stimulated twice in succession. Multiple sites close to equipment is to the right in the image; however, in cases of right-sided one another were chosen on the cortex exposed by the tumors, some of this equipment must be moved to the left side of the OR. craniotomy. Usually, 4–6 mA is the maximum stimulus needed to localize the language center, whereas up to 10 mA is needed to localize the motor cortex. Subcortical eration of critical anesthetic equipment. The team must stimulation is performed with either the Ojemann (bipo- be creative in positioning and draping the patient, since lar) stimulator or the Prass probe (monopolar) stimulator. standard OR arm boards and intravenous poles are not The Prass probe, train of 5 at 500 Hz, duration of 0.5 MRI compatible. Figure 2 shows a patient being tested msec, with currents ranging from 2 to 20 mA, is used to with picture cards during the awake procedure. There elicit a motor response. is ready access to the patient if reintubation is required, In patients in whom language sites are identified, the and interactions among the surgeon, anesthesiologist, and resection margin is taken within 1–2 cm of cortical areas patient are enhanced by the plastic drapes, which allow important for speech function. In patients in whom the pri- additional lighting. Besides the operating surgeon and mary motor and sensory cortices are mapped, the resection the scrub nurse, there are two anesthesia and two nurs- margin is taken closer to the cortical margins (up to 0.5 ing staff in the OR at all times during the operation to cm). The resection is stopped if speech function deterio- facilitate communication and lend assistance as needed. rates but is resumed if full recovery occurs within 5 min- Cortical and Subcortical Stimulation utes. During cortical stimulation, simultaneous recording with electrocorticography is not performed because of the Immediately before tumor resection, the patient is tailored craniotomy openings in these patients. awakened and, after the LMA is removed, can easily communicate with the neuroanesthesiologist and the sur- Magnetic Resonance Imaging Studies The integrated MRI OR (Brainlab AG) includes a 1.5-T MRI scanner (Magnetom Espree, Siemens) that is integrated with the VectorVision Sky neuronavigation system (Brainlab AG) in a specially designed OR with radiofrequency shielding. It is equipped with a rotating table attached to the 1.5-T MRI scanner that allows the patient’s head to be placed outside the 5-gauss line during surgery. Ordinary surgical instruments can be used out- side this line. The high-field scanner consists of a super- conductive 1.5-T magnet with a length of 160 cm and an inner bore diameter of 70 cm. Both pre- and intraopera- tive imaging are performed with this magnet. All equip- ment that is not MRI compatible, such as the operating microscope, intraoperative ultrasonography apparatus, and surgeon’s chair, remain outside the 5-gauss line and are mechanically secured to the wall or ceiling of the OR. An MRI-compatible respirator and anesthesia care moni- tor are used. Drug infusion continues via infusion pumps Fig. 2. A patient is tested with picture cards during the awake pro- cedure. There is ready access to the patient if reintubation is required, while the intraoperative images are obtained. and interactions among the surgeon, anesthesiologist, and patient are The different types of imaging sequences obtained enhanced by the plastic drapes, which allow additional lighting and pa- preoperatively and intraoperatively include a registration tient comfort. scan, diffusion tensor imaging (DTI), FLAIR, T2-weight-

812 J Neurosurg / Volume 121 / October 2014 Awake craniotomy in intraoperative MRI ed, and diffusion-weighted imaging (DWI). Preoperative spectroscopy and high-resolution DTI (pre- and/or post- operatively) are performed at the surgeon’s discretion. A contrast agent is also used at the discretion of the surgeon and the neuroradiologist. Preoperative scanning is per- formed after laryngeal mask intubation and positioning of the patient. A 3D data set is obtained using iMRI. Im- aging procedures include the following sequences: T1- weighted spin echo: section thickness 1.3 mm, FOV 230 mm2, TE 2.5 msec, TR 5 msec, scan time 2 minutes 59 seconds; T2-weighted turbo spin echo: section thickness 1 mm, FOV 230 mm2, TE 447 msec, TR 3000 msec, scan time 4 minutes 24 seconds; FLAIR: section thickness 1.5 mm, FOV 230 mm2, TE 397 msec, TR 6000 msec, scan time 5 minutes 56 seconds; DTI: section thickness 4 mm, FOV 230 mm2, TE 106 msec, TR 3500 msec, scan time 5 minutes 38 seconds; and DWI: section thickness 4 mm, FOV 230 mm2, TE 96 msec, TR 4500 msec, scan time 2 minutes 20 seconds. If the tumor demonstrates contrast enhancement in preoperative studies, the T1- weighted spin echo sequence is repeated after intrave- nous administration of gadopentetate dimeglumine (0.2 Fig. 3. Presurgical planning image obtained in a left-hand dominant ml/kg, Magnevist, Berlex/Schering). Diffusion tensor and patient with a right, frontal, nonenhancing anaplastic glioma. On the diffusion-weighted imaging sequences are obtained to lo- 3D volume-rendered image, the tumor is yellow, the fMRI overlay for calize nearby white matter fiber tracts and detect early is- speech is purple, and the fMRI overlay for motor function is orange. The chemia. Note that in every case the surgeon and the neu- corticospinal tract and the inferior occipitofrontal fasciculus are also roradiologist will confer on the best sequences to guide overlaid (purple and blue). tumor resection. The desired sequences are automatically registered to the ceiling-mounted navigation system (Cra- procedures using iMRI were performed in 41 patients, 25 nial 7.8 software, Brainlab). No skin fiducial markers are males and 16 females, with a median age of 41.2 years needed. Data from functional MRI (fMRI) performed (range 22–70 years; Table 1). Newly diagnosed tumors 1–2 days before surgery can also be integrated into the were treated in 36 procedures (85.7%) and recurrent tu- 3D data set for intraoperative functional neuronavigation mors in 6 (14.3%). The majority of tumors (73.8%) were (Figs. 3 and 4). on the left side. Nine procedures (21.4%) were performed The surgeon can obtain intraoperative images for re- for multiforme, 19 for anaplastic gliomas registration or to verify that the resection is complete. If (42.9%), and 14 for low-grade gliomas (35.7%). Most tu- residual tumor is identified, the navigation system can be updated with new anatomical and functional data, such as those obtained with DTI (Fig. 5). Further tumor resection is performed unless there is a risk of damaging eloquent brain regions. Control postoperative MRI scans are acquired either at the completion of surgery or within 48 hours after sur- gery. The system for this postoperative imaging uses a standard 1.5-T General Electric magnet. Postoperative Neurological Evaluation Postoperative evaluation of neurological outcome was performed after the surgery and at the 1-month fol- low-up examination. The pre- and postoperative Karnof- sky Performance Scale scores were also registered. Statistical Analysis Comparisons between groups were performed using a t-test, and p = 0.05 was considered to be significant.

Results Fig. 4. Intraoperative navigation screenshot showing the position of Patient and Tumor Characteristics the navigation probe (green line and cross-hairs) at the inferior margin of the tumor. The patient experienced semantic errors during stimula- In the defined study period, 42 awake craniotomy tion, indicating proximity to the inferior occipitofrontal fasciculus.

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TABLE 1: Summary of patient and tumor characteristics in those undergoing awake craniotomy

Characteristic No. median age in yrs (range) 41.2 (22–70) sex (%) M 25 (60) F 16 (40) side of lesion (%) lt 31 (74) rt 11 (26) tumor location (%) frontal lobe 17 (40.5) frontal & adjacent lobe 5 (11.9) temporal lobe 5 (11.9) temporal & adjacent lobe 4 (9.5) parietal lobe 4 (9.5) insular (true) 2 (4.8) Fig. 5. Intraoperative scans showing a very small amount of residual insular (temporal/frontal) 5 (11.9) tumor (yellow) at the anterosuperior portion of the resection cavity. This relationship w/ eloquent brain areas (%) residual tumor was resected, and GTR of the tumor seen in Figs. 3 and 4 was achieved. speech only 9 (21.4) motor only 12 (28.6) mors were located in the frontal lobe (40.5%) and the speech & motor 21 (50) frontal lobe with extension to adjacent areas (11.9%), fol- newly diagnosed (%) 36 (85.7) lowed by tumors in the temporal lobe (11.9%), temporal lobe with extension to adjacent areas (9.5%), and the pa- recurrent (%) 6 (14.3) rietal lobe (9.5%). A purely insular location was seen in histology (%) 2 cases, and a combination of insular and its adjacent re- high-grade glioma 28 (67) gions (frontal and/or temporal) was seen in 5 cases. In 21 low-grade glioma 14 (33) cases the lesion was related to both the motor and speech mean preop tumor vol in cm3 (range) 49 (3.3–154.2) cortices, 12 cases to the motor cortex, and 9 cases to the speech cortex. The mean preoperative tumor volume was 49 cm3 (range 3.3–154.2). Among the 41 patients in whom the craniotomy procedure was performed, preoperative insular versus noninsular (35) tumor cases was 10.9 ± 1.4 neurological deficits were identified in 9 patients (21.9%). hours and 6.3 ± 1.00 hours, respectively. Six cases (66.7%) were speech related, 2 (22.2%) were Other variables included in total surgery time were motor deficits, and combined deficits (speech and motor) the time that a patient spent awake and any time required were found in 1 patient (11.1%). to replace the LMA. The mean awake time during sur- gery was 2.8 hours overall (range 0.6–7.9 hours), 2.6 Surgery Time hours for patients with low-grade tumors, and 2.9 hours Surgery time was calculated from the time of initial for those with high-grade tumors, with no significant dif- skin incision to complete closure of the wound, including ference between the latter two (p = 0.60). direct electrical stimulation mapping, resection, intraop- Some patients were reintubated with the LMA device erative imaging, and any subsequent resection of residual for the remainder of the procedure following direct elec- tumor if deemed necessary after image review. The mean trical stimulation mapping. This decision was based on surgery time was 7.3 hours overall (range 4.0–13.9 hours; the anesthesiologist and neurosurgeon preferences. In the Table 2), 7.8 hours for low-grade tumors, and 7.0 hours for 42 procedures, reintubation with LMA device replace- high-grade tumors; there was no statistically significant ment occurred in 33 cases (78.6%). difference between the latter two (p = 0.27). The mean Scan Times surgery time was 6.5 hours for patients who required only 1 intraoperative scan and 8.0 hours for those with residual The mean total scan time for patients, including pre- tumors requiring reintervention and subsequent postoper- operative, intraoperative, and second intraoperative scans, ative scanning, although there was no statistically signifi- was 25.3 minutes (range 5.3–58.0 minutes). The mean time cant difference between the two (p = 0.27). Total surgery for preoperative scanning (42 cases) was 9.0 minutes (range time exceeded 8 hours in 10 patients, including 5 patients 4.1–32.0 minutes; Table 2). The mean time for intraopera- with low-grade tumors and 5 patients with high-grade tu- tive scanning (39 cases) was 15.6 minutes (range 5.1–27.1 mors. In these 10 patients, 7 surgeries were performed for minutes). The mean time for a second intraoperative scan tumors in the insular area. The mean surgery time for the (10 cases) was 7.7 minutes (range 1.1–11.2 minutes).

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TABLE 2: Summary of intraoperative data in patients undergoing none of these 12 cases developed worsening neurological awake craniotomy deficits. Hence, the combination of iMRI and mapping used in a complementary fashion benefited 12 (28.6%) of Parameter Value 42 cases in this study. mean surgery time in hrs (range) 7.3 (4–13.9) We specifically questioned why an STR or a PR was mean awake time in hrs (range) 2.8 (0.6–7.9) performed in 25 cases. In 4 of the 25 cases, the surgeon and neuroradiologist believed that a GTR had been achieved mean scanning time in mins (range) following the intraoperative scan; however, on postopera- preop (42 cases) 9.0 (4.1–32.0) tive volumetric measurements, it became evident that the intraop (39 cases) 15.6 (5.1–27.1) resections were actually subtotal. An intraoperative defi- 2nd intraop (10 cases) 7.7 (1.1–11.2) cit in 4 cases, bifrontal tumors in 5 cases, and intraopera- intraop (%) 3 (7) tive seizures in 2 cases prevented additional resection. In 10 of the 25 cases unforeseen intraoperative anatomical constraints also prevented additional resection (Table 4). In 3 cases no intraoperative scan was performed: In Anesthesia and Awake Craniotomy 2 of these cases the surgeon believed that an intraopera- tive scan would not change the course of surgery, and in The LMA device was reinserted in 33 (78.6%) of 42 1 patient intraoperative seizures prevented resection, and procedures after the surgeon believed that the goals of hence a scan was not performed. surgery had been met. In all of these cases, careful posi- The total number of sequences per patient per pro- tioning of the neck preoperatively prevented any reintu- cedure was 5.8 overall (range 2–11 sequences), with an bation problems. In 10 (25.6%) of 39 procedures, patients average of 5.2 sequences for the low-grade tumor group were awake during intraoperative scanning and remained and 6.1 sequences for the high-grade tumor group. There cooperative. In 17 of 42 cases further resection was nec- was no statistically significant difference in the number essary, and in 6 of these cases the patients were reawak- of sequences per patient per procedure between the low- ened after the scanning. grade and high-grade tumor groups (p = 0.19). Seizures Extent of Resection Three patients (7%) had intraoperative seizures, and In the 14 low-grade tumor surgeries, gross-total re- only 1 of them had a GTR after the seizures were con- section (GTR; defined as ≥ 95% volumetric resection) trolled. In the other 2 patients, who had tumors in the was accomplished in 5 cases (35.7%; Table 3). One (7.1%) motor gyrus, repeated seizures resulted in only PR of the of 14 cases underwent subtotal resection (STR; defined as tumors. 85% to < 95% volumetric resection), and 8 (57.1%) of 14 underwent partial resection (PR; defined as < 85% volu- Neurological Outcomes metric resection). New or worsening neurological deficits were ob- In the 28 high-grade tumor surgeries, GTR was ac- served in 11 (26%) of 42 cases immediately after surgery. complished in 12 cases (42.8%). Six cases (21.4%) under- At the 1-month follow-up, however, only 1 patient (2.4%) went STR, and 10 cases (35.7%) underwent PR. had a new or worsened neurological deficit. There was no statistically significant difference in the average EOR between low-grade and high-grade tu- mors (p = 0.31). Overall, in the 42 procedures, 17 (40.5%) Discussion resulted in GTR, 7 (16.7%) in STR, and 18 (42.8%) in The use of iMRI for the safe maximal resection of in- PR. The median EOR overall was 90.0%, with a mean of trinsic brain tumors is well established; however, studies 76.0%. After the first intraoperative scan, only 10 cases showing the utility of both low-field and high-field (1.5 T) (24%) resulted in GTR, with the rate increasing to 17 iMRI for awake craniotomy procedures and the associ- cases (40.5%) after re-resection. Hence, in 7 (41%) of 17 ated challenges are limited.2,3,11–14,18,22–24 In some earlier cases, iMRI helped to achieve a GTR. In the 17 patients who had a re-resection, the mean EOR increased from TABLE 4: Reasons for resection ≤ 85% in 25 cases 56% to 67%. Of the 17 cases of re-resection, 12 had a ≥ resection 85%; of these 12 cases, 7 had a GTR. Notably, Reason No. (%) TABLE 3: Extent of resection in 42 gliomas surgeon believed that GTR achieved 4 (16) intraop deficit 4 (16) EOR No. (%) bifrontal tumor 5 (20) GTR (≥95% volumetric resection) 17 (40.5%) seizures 2 (8) STR (85% to <95% volumetric resection) 7 (16.7) anatomical limiting factors* 10 (40) PR (<85% volumetric resection) 18 (42.8) STR & PR 25 (59.5) * For example, undue retraction on blood vessels and eloquent brain, difficulty splitting the sylvian fissure, tumor infiltrating eloquent cortical iMRI helped achieve GTR 7/17 (41) and subcortical structures, and so forth.

J Neurosurg / Volume 121 / October 2014 815 M. V. C. Maldaun et al. work we showed that intraoperative multimodality elec- one-third of the cases (29%), the iMRI and mapping tech- trophysiological mapping can be seamlessly incorporated niques were complementary in achieving a safe maximal into high-field iMRI for tumor resections.15 Initially when resection of the tumor without causing any additional we started the procedure of combining awake craniotomy neurological decline. Because of the limited access to a with high-field iMRI, there were a number of challenges patient’s airway in the iMRI suite as compared with the to overcome, including patient comfort and position as regular OR, the occurrence of seizures is a concern. In well as new draping and anesthetic techniques unique to this study 3 patients (7%) had seizures, which is compa- the iMRI environment. rable to the rate (9%) in our large series of 309 patients Of the 6 awake craniotomy studies on high-field previously described.8 In all 3 cases the anesthesiologist iMRI published in the literature thus far, ours represents had good and ready access to the patient airway and con- the largest patient experience (Table 5).3,11,12,13,24 In the se- trolled the seizures without any additional complications. ries described by Leuthardt et al.11 and the case report by In 1 of these cases, a GTR was achieved; however, in the Parney et al.,13 an overhead moveable magnet was used other 2 cases with intraoperative seizures, the tumors for scanning. However, in the other series,3,12,24 including were in the motor gyrus and were only partially resected. ours, the position of the magnet was fixed on the floor, High-field iMRI provides excellent-quality images and the patient was moved toward the scanner for intra- that can assist the surgeon with both preoperative and in- operative scans. The overall operative time in our patient traoperative planning. Incorporating overlaid presurgical population was 7.3 hours, which is longer than the times mapping images, including fMRI, DTI, and, more recent- reported in the other published studies. In our study, how- ly, the deformable anatomical template9 and navigated ever, 7 (17%) of 42 cases had tumors primarily in the in- transcranial magnetic stimulation data, into the workflow sular region and a combination of insular and adjacent can also aid surgical planning. The system software al- frontal and temporal lobes, requiring longer operative lows for automatic registration during rescanning, which times (10.9 ± 1.4 hours). For tumors outside the insular expedites the workflow. region (35 cases), the mean operative time was 6.3 ± 1.00 The use of iMRI was beneficial in achieving a more hours, which is more acceptable given the technology of complete resection given the proximity of these tumors to the high-field iMRI. Moreover, the mean awake time dur- eloquent cortex. After the first intraoperative scan, only 10 ing surgery was 2.8 hours overall (range 0.6–7.9 hours), cases (24%) had GTR, which increased to 17 cases (35.7%) with patients harboring insular tumors being awake the after re-resection. Hence in 7 (41%) of 17 cases, the iMRI longest. In 42 awake procedures, there were no adverse helped to achieve GTR. In 25 cases a GTR could not be events that occurred to either the patient or personnel. achieved. In a majority of these cases (10 [40%] of 25) un- The mean total scan time for patients, including pre- foreseen intraoperative anatomical constraints (for exam- operative, intraoperative, and (if needed) second intraop- ple, undue retraction on blood vessels and eloquent brain, erative scanning, was 25.3 minutes (range 5.3–58.0 min- difficulty splitting the sylvian fissure, tumor infiltrating utes) and did not seem to significantly compromise total eloquent cortical and subcortical structures, and so forth) operative times. During rescanning, the upper coil must prevented additional resection from being performed. This be replaced, requiring excellent compliance and coopera- highlights the challenge when operating in eloquent re- tion from the patient since they have limited visibility in gions of the brain despite the use of iMRI. Nonetheless, ex- the scanner. We have been successful in keeping almost cellent neurological outcomes were achieved in this study, one-third (25.6%) of the patients awake during intraop- with only 1 patient (2.4%) having a new or worsened neu- erative scanning without any reported problems. Of the rological deficit at the 1-month follow-up. 17 patients who required a re-resection, 6 of them were reawakened after the intraoperative scan, with no diffi- Conclusions culties. In 10 of these 17 patients, however, the surgeon felt that the remainder of the resection could be safely We have demonstrated that awake craniotomy in the performed while the patient was asleep, as the residual high-field (1.5 T) iMRI setting is a safe and useful means tumor was in a safe area for re-resection. Hence, in almost of maximizing EOR with a lower incidence of postopera-

TABLE 5: Summary of studies on awake craniotomy in high-field iMRI*

Mean Op Time in Mean No. of Intraop Mean Scanning Time Anesthesia Authors & Year No. of Procedures Hrs (range) Scans (range) in Mins (range) Technique Weingarten et al., 2009 10 6.8 (3.8–8.7) 2 (1–3) (30–40)† IV Nabavi et al., 2009 38 NR NR (20–60)† IV Goebel et al., 2010 25 (4–5.5)† 1.4 (0–2) NR IV Leuthardt et al., 2011 12 4.76 (2.7–6.02) NR 44.4 (28.8–69) LMA + IV Parney et al., 2010 1 NR NR NR IV present case 42 7.3 (4.0–13.9) 1.2 (0–2) 25.3 (5.3–58.0) LMA + IV

* Field strength of iMRI was 1.5 T in all studies. IV = intravenous; NR = not reported. † Mean not specified.

816 J Neurosurg / Volume 121 / October 2014 Awake craniotomy in intraoperative MRI tive neurological deficits. Intraoperative navigation and magnetic resonance imaging with awake craniotomies for electrophysiological monitoring can be seamlessly incor- resection of gliomas: preliminary experience. Neurosurgery porated into the OR with no adverse events to patients. 69:194–206, 2011 12. Nabavi A, Goebel S, Doerner L, Warneke N, Ulmer S, Me- hdorn M: Awake craniotomy and intraoperative magnetic res- Disclosure onance imaging: patient selection, preparation, and technique. The authors report no conflict of interest concerning the mate- Top Magn Reson Imaging 19:191–196, 2009 rials or methods used in this study or the findings specified in this 13. Parney IF, Goerss SJ, McGee K, Huston J III, Perkins WJ, paper. Meyer FB: Awake craniotomy, electrophysiologic mapping, Author contributions to the study and manuscript preparation and tumor resection with high-field intraoperative MRI.World include the following. Conception and design: Prabhu, Maldaun, Neurosurg 73:547–551, 2010 Khawja. Acquisition of data: Prabhu, Maldaun, Khawja. Analysis 14. Peruzzi P, Puente E, Bergese S, Chiocca EA: Intraoperative and interpretation of data: Prabhu, Maldaun, Khawja. Drafting MRI (ioMRI) in the setting of awake craniotomies for supra- the article: all authors. Critically revising the article: all authors. tentorial glioma resection. Acta Neurochir Suppl 109:43– Reviewed submitted version of manuscript: all authors. Approved 48, 2011 the final version of the manuscript on behalf of all authors: Prabhu. 15. 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