✓ The authors describe the use of stereoscopic short-range magnetic resonance (MR) angiography to diagnose whether and by what means the brainstem is compressed in a case of facial spasm. The MR images were obtained on a 1.5-tesla imaging system with three-dimensional time-of-flight pulse sequence (repetition time 39 msec, echo time 9 msec). Six-source MR images, in which the internal acoustic meatuses were described, were processed using a maximum-intensity projection technique to reconstruct the MR angiograms. The internal acoustic meatuses, the posterior fossa, and the nearby arteries are shown on a single MR angiogram. When two MR angiograms with projection angles 10° apart are placed side by side and observed through polarized glasses, a stereoscopic view of the compressing artery can easily be seen.
Takashi Shimizu, Hiroto Kawasaki, Hidetoshi Kasuya and Koki Kurita
Hans E. Bakken, Hiroto Kawasaki, Hiroyuki Oya, Jeremy D. W. Greenlee and Matthew A. Howard III
✓ Neurosurgeons use invasive mapping methods during surgery to understand the functional neuroanatomy of patients. Electrical stimulation methods are used routinely for the temporary disruption of focal regions of cerebral cortex so that the surgeon may infer the functional role of the brain site being stimulated. Although it is an efficient and useful method, modes of electrical stimulation mapping have significant limitations. Neuroscientists use focal cooling to effect a more controlled disruption of cortical functions in experimental animals, and in this report, the authors describe their experience using a device to achieve this same objective in patients undergoing neurosurgery. The cooling probe consists of a stainless steel chamber with thermocouples and electroencephalography (EEG) recording contacts. Active cooling is achieved by infusing chilled saline into the chamber when the cooling probe is positioned on the pial surface. Experiments were performed in 18 patients. Temperature gradient measurements indicate that the entire thickness of gray matter under the probe is cooled to temperatures that disrupt local synaptic activity. Statistically significant changes in spontaneous and stimulusevoked EEG activity were consistently observed during cooling, providing clear evidence of reversible disruption of physiological functions. Preliminary findings during functional mapping of the Broca area demonstrated qualitative differences between the temporary neurological deficits induced by cooling and those caused by electrical stimulation. These findings indicate the safety and utility of the cooling probe as a neurosurgical research tool. Additional rigorously designed studies should be undertaken to correlate the effects of cooling, electrical stimulation, and focal lesioning.
Chandan G. Reddy, Goutam G. Reddy, Hiroto Kawasaki, Hiroyuki Oya, Lee E. Miller and Matthew A. Howard III
Control signals for brain-machine interfaces may be obtained from a variety of sources, each with their own relative merits. Electrocorticography (ECoG) provides better spatial and spectral resolution than scalp electroencephalography and does not include the risks attendant upon penetration of the brain parenchyma associated with single and multiunit recordings. For these reasons, subdural electrode recordings have been proposed as useful primary or adjunctive control signals for brain-machine interfaces. The goal of the present study was to determine if 2D control signals could be decoded from ECoG.
Six patients undergoing invasive monitoring for medically intractable epilepsy using subdural grid electrodes were asked to perform a motor task involving moving a joystick in 1 of 4 cardinal directions (up, down, left, or right) and a fifth condition (“trigger”). Evoked activity was synchronized to joystick movement and analyzed in the theta, alpha, beta, gamma, and high-gamma frequency bands.
Movement-related cortical potentials could be accurately differentiated from rest with very high accuracy (83–96%). Further distinguishing the movement direction (up, down, left, or right) could also be resolved with high accuracy (58–86%) using information only from the high-gamma range, whereas distinguishing the trigger condition from the remaining directions provided better accuracy.
Two-dimensional control signals can be derived from ECoG. Local field potentials as measured by ECoG from subdural grids will be useful as control signals for a brain-machine interface.
Yasunori Nagahama, Brian J. Dlouhy, Daichi Nakagawa, Janina Kamm, David Hasan, Matthew A. Howard III and Hiroto Kawasaki
Intracranial electroencephalography (iEEG) provides invaluable information in determining seizure focus and spread due to its high spatial and temporal resolution, which are not afforded by noninvasive studies. Electrodes of various types (e.g., grid, strip, and depth electrodes) and configurations are often used for optimum coverage of suspected areas of seizure onset and propagation. Given the fixed intracranial volume and added mass effect from placement of cortical electrodes, brain edema and postoperative deficits can occur.
The authors describe a simple, inexpensive, and highly effective technique of bone flap replacement using standard titanium plates to expand the intracranial volume and minimize risks of brain compression and intracranial hypertension. Rectangular titanium plates are bent and placed in a way that secures the bone flap in a slightly elevated position relative to the adjacent calvaria during iEEG monitoring. The authors evaluated the degree of bone flap elevation and amount of volume created using this technique in 3 iEEG cases. They then compared these results with the bone flap elevation and volume created using linear titanium plates, a method they had used previously. The use of rectangular plates produced on average 6.6 mm of bone flap elevation, compared with only 1.8 mm of bone flap elevation with the use of linear plates, resulting in a statistically significant 261% increase in bone flap elevation (p ≤ 0.001). The authors suggest that rectangular plates may provide stronger resistance to scalp tension after myocutaneous skin closure compared with the linear plates and that subsidence of the bone flap likely occurred with the use of linear plates. In summary, the described technique utilizing rectangular plates creates significantly increased bone flap elevation compared with a similar method using linear plates, and it may reduce the risk of neurological deficits related to intracranial electrode placement.
Brian J. Dlouhy, Steven V. Viljoen, David K. Kung, Timothy W. Vogel, Mark A. Granner, Matthew A. Howard III and Hiroto Kawasaki
Vagus nerve stimulation (VNS) has demonstrated benefit in patients with medically intractable partial epilepsy. As in other therapies with mechanical devices, hardware failure occurs, most notably within the VNS lead, requiring replacement. However, the spiral-designed lead electrodes wrapped around the vagus nerve are often encased in dense scar tissue hampering dissection and removal. The objective in this study was to characterize VNS lead failure and lead revision surgery and to examine VNS efficacy after placement of a new electrode on the previously used segment of vagus nerve.
The authors reviewed all VNS lead revisions performed between October 2001 and August 2011 at the University of Iowa Hospitals and Clinics. Twenty-four patients underwent 25 lead revisions. In all cases, the helical electrodes were removed, and a new lead was placed on the previously used segment of vagus nerve. All inpatient and outpatient records of the 25 lead revisions were retrospectively reviewed.
Four cases were second lead revisions, and 21 cases were first lead revisions. The average time to any revision was 5 years (range 1.8–11.1 years), with essentially no difference between a first and second lead revision. The most common reason for a revision was intrinsic lead failure resulting in high impedance (64%), and the most common symptom was increased seizure frequency (72%). The average duration of surgery for the initial implantation in the 15 patients whose VNS system was initially implanted at the authors' institution was much shorter (94 minutes) than the average duration of lead revision surgery (173 minutes). However, there was a significant trend toward shorter surgical times as more revision surgeries were performed. Sixteen of the 25 cases of lead revision were followed up for more than 3 months. In 15 of these 16 cases, the revision was as effective as the previous VNS lead. In most of these cases, both the severity and frequency of seizures were decreased to levels similar to those following the previous implantation procedure. Only 1 complication occurred, and there were no postoperative infections.
Lead revision surgery involving the placement of a new electrode at the previously used segment of vagus nerve is effective at decreasing the seizure burden to an extent similar to that obtained following the initial VNS implantation. Even with multiple lead revisions, patients can obtain VNS efficacy similar to that following the initial lead implantation. There is a learning curve with revision surgery, and overall the duration of surgery is longer than for the initial implantation. Note, however, that complications and infection are rare.
Gregory W. Albert, Nader S. Dahdaleh, Chandan Reddy, Daniel R. Hansen, Timothy W. Vogel, Hiroto Kawasaki and Matthew A. Howard III
In this study the authors sought to determine whether any correlations existed between postimplantation head CT findings and the need to perform decompression surgery in patients with grid electrodes.
The authors identified 74 patients who underwent intracranial electrode monitoring for medically refractory epilepsy from January 2000 through June 2008. Only the 46 patients who had head CT scans available for review were included in the study. The authors were able to determine the number and types of electrodes placed as well as complications experienced. They reviewed the CT scans for abnormal findings including extraaxial fluid collections, intracranial hemorrhages, and signs of mass effect.
All patients developed some degree of extraaxial fluid collection following the placement of intracranial electrodes. The maximum width of the extraaxial fluid collection and the degree of midline shift were not predictive of the need for decompressive surgery. The presence, but not degree, of midline shift was associated with the need for decompressive surgery. Likewise, the presence of ventricular asymmetry was correlated with the need for removal of the electrodes and bone flap. Patients without midline shift or ventricular asymmetry on CT did not require decompressive surgery.
After undergoing placement of intracranial electrodes all patients develop extraaxial fluid collections. In addition, many patients develop signs of mass effect including midline shift and ventricular asymmetry. When these findings are absent it is highly unlikely that surgical decompression is required.
Yasunori Nagahama, Alan J. Schmitt, Daichi Nakagawa, Adam S. Vesole, Janina Kamm, Christopher K. Kovach, David Hasan, Mark Granner, Brian J. Dlouhy, Matthew A. Howard III and Hiroto Kawasaki
Intracranial electroencephalography (iEEG) provides valuable information that guides clinical decision-making in patients undergoing epilepsy surgery, but it carries technical challenges and risks. The technical approaches used and reported rates of complications vary across institutions and evolve over time with increasing experience. In this report, the authors describe the strategy at the University of Iowa using both surface and depth electrodes and analyze outcomes and complications.
The authors performed a retrospective review and analysis of all patients who underwent craniotomy and electrode implantation from January 2006 through December 2015 at the University of Iowa Hospitals and Clinics. The basic demographic and clinical information was collected, including electrode coverage, monitoring results, outcomes, and complications. The correlations between clinically significant complications with various clinical variables were analyzed using multivariate analysis. The Fisher exact test was used to evaluate a change in the rate of complications over the study period.
Ninety-one patients (mean age 29 ± 14 years, range 3–62 years), including 22 pediatric patients, underwent iEEG. Subdural surface (grid and/or strip) electrodes were utilized in all patients, and depth electrodes were also placed in 89 (97.8%) patients. The total number of electrode contacts placed per patient averaged 151 ± 58. The duration of invasive monitoring averaged 12.0 ± 5.1 days. In 84 (92.3%) patients, a seizure focus was localized by ictal onset (82 cases) or inferred based on interictal discharges (2 patients). Localization was achieved based on data obtained from surface electrodes alone (29 patients), depth electrodes alone (13 patients), or a combination of both surface and depth electrodes (42 patients). Seventy-two (79.1%) patients ultimately underwent resective surgery. Forty-seven (65.3%) and 18 (25.0%) patients achieved modified Engel class I and II outcomes, respectively. The mean follow-up duration was 3.9 ± 2.9 (range 0.1–10.5) years. Clinically significant complications occurred in 8 patients, including hematoma in 3 (3.3%) patients, infection/osteomyelitis in 3 (3.3%) patients, and edema/compression in 2 (2.2%) patients. One patient developed a permanent neurological deficit (1.1%), and there were no deaths. The hemorrhagic and edema/compression complications correlated significantly with the total number of electrode contacts (p = 0.01), but not with age, a history of prior cranial surgery, laterality, monitoring duration, and the number of each electrode type. The small number of infectious complications precluded multivariate analysis. The number of complications decreased from 5 of 36 cases (13.9%) to 3 of 55 cases (5.5%) during the first and last 5 years, respectively, but this change was not statistically significant (p = 0.26).
An iEEG implantation strategy that makes use of both surface and depth electrodes is safe and effective at identifying seizure foci in patients with medically refractory epilepsy. With experience and iterative refinement of technical surgical details, the risk of complications has decreased over time.
Yasunori Nagahama, Christopher K. Kovach, Michael Ciliberto, Charuta Joshi, Ariane E. Rhone, Adam Vesole, Phillip E. Gander, Kirill V. Nourski, Hiroyuki Oya, Matthew A. Howard III, Hiroto Kawasaki and Brian J. Dlouhy
Musicogenic epilepsy (ME) is an extremely rare form of the disorder that is provoked by listening to or playing music, and it has been localized to the temporal lobe. The number of reported cases of ME in which intracranial electroencephalography (iEEG) has been used for seizure focus localization is extremely small, especially with coverage of the superior temporal plane (STP) and specifically, Heschl’s gyrus (HG). The authors describe the case of a 17-year-old boy with a history of medically intractable ME who underwent iEEG monitoring that involved significant frontotemporal coverage as well as coverage of the STP with an HG depth electrode anteriorly and a planum temporale depth electrode posteriorly. Five seizures occurred during the monitoring period, and a seizure onset zone was localized to HG and the STP. The patient subsequently underwent right temporal neocortical resection, involving the STP and including HG, with preservation of the mesial temporal structures. The patient remains seizure free 1 year postoperatively. To the authors’ knowledge, this is the first reported case of ME in which the seizure focus has been localized to HG and the STP with iEEG monitoring. The authors review the literature on iEEG findings in ME, explain their approach to HG depth electrode placement, and discuss the utility of STP depth electrodes in temporal lobe epilepsy.
Chandan G. Reddy, Nader S. Dahdaleh, Gregory Albert, Fangxiang Chen, Daniel Hansen, Kirill Nourski, Hiroto Kawasaki, Hiroyuki Oya and Matthew A. Howard III
A wide range of devices is used to obtain intracranial electrocorticography recordings in patients with medically refractory epilepsy, including subdural strip and grid electrodes and depth electrodes. Penetrating depth electrodes are required to access some brain regions, and 1 target site that presents a particular technical challenge is the first transverse temporal gyrus, or Heschl gyrus (HG). The HG is located within the supratemporal plane and has an oblique orientation relative to the sagittal and coronal planes. Large and small branches of the middle cerebral artery abut the pial surface of the HG and must be avoided when planning the electrode trajectory.
Auditory cortex is located within the HG, and there are functional connections between this dorsal temporal lobe region and medial sites commonly implicated in the pathophysiology of temporal lobe epilepsy. At some surgical centers, depth electrodes are routinely placed within the supratemporal plane, and the HG, in patients who require intracranial electrocorticography monitoring for presumed temporal lobe epilepsy. Information from these recordings is reported to facilitate the identification of seizure patterns in patients with or without auditory auras.
To date, only one implantation method has been reported to be safe and effective for placing HG electrodes in a large series of patients undergoing epilepsy surgery. This well-established approach involves inserting the electrodes from a lateral trajectory while using stereoscopic stereotactic angiography to avoid vascular injury. In this report, the authors describe an alternative method for implantation. They use frameless stereotaxy and an oblique insertion trajectory that does not require angiography and allows for the simultaneous placement of subdural grid arrays. Results in 19 patients demonstrate the safety and efficacy of the method.
Taylor J. Abel, Royce W. Woodroffe, Kirill V. Nourski, Toshio Moritani, Aristides A. Capizzano, Patricia Kirby, Hiroto Kawasaki, Matthew Howard III and Mary Ann Werz
A convergence of clinical research suggests that the temporal pole (TP) plays an important and potentially underappreciated role in the genesis and propagation of seizures in temporal lobe epilepsy (TLE). Understanding its role is becoming increasingly important because selective resections for medically intractable TLE spare temporopolar cortex (TPC). The purpose of this study was to characterize the role of the TPC in TLE after using dense electrocorticography (ECoG) recordings in patients undergoing invasive monitoring for medically intractable TLE.
Chronic ECoG recordings were obtained in 10 consecutive patients by using an array customized to provide dense coverage of the TP as part of invasive monitoring to localize the epileptogenic zone. All patients would eventually undergo cortico-amygdalohippocampectomy. A retrospective review of the patient clinical records including ECoG recordings, neuroimaging studies, neuropathology reports, and clinical outcomes was performed.
In 7 patients (70%), the TP was involved at seizure onset; in 7 patients (70%), there were interictal discharges from the TP; and in 1 case, there was early spread to the TP. Seizure onset in the TP did not necessarily correlate with preoperative neuroimaging abnormalities of the TP.
These data demonstrate that TPC commonly plays a crucial role in temporal lobe seizure networks. Seizure onset from the TP would not have been predicted based on available neuroimaging data or interictal discharges. These findings illustrate the importance of thoroughly considering the role of the TP prior to resective surgery for TLE, particularly when selective mesial resection is being considered.