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Alon Y. Mogilner and Ali R. Rezai

Chronic epidural motor cortex stimulation (MCS) has been shown to have promise in the treatment of patients with refractory deafferentation pain. Precise placement of the electrode over the motor cortex region corresponding to the area of pain is essential for the success of this procedure. Whereas standard anatomical landmarks have been used in the past in conjunction with image guidance, the use of functional brain imaging can be beneficial in the precise surgical planning. The authors report the use of functional imaging–guided frameless stereotactic surgery for epidural MCS. Five patients underwent MCS in which functional imaging guidance was used. Prior to surgery, patients underwent magnetic resonance (MR) imaging with skin fiducial markers placed on standard anatomical reference prints, followed by magnetoencephalography (MEG) mapping of the sensory and motor cortices. In two patients, functional MR imaging was also performed using a motor task paradigm. The functional imaging data were integrated into a frameless stereotactic database by using a three-dimensional coregistration algorithm. Subsequently, a frameless stereotactic craniotomy was performed using the integrated anatomical and functional imaging data for surgical planning. Intraoperative somatosensory evoked potentials (SSEPs) and direct stimulation were used to confirm the target and final placement of the electrode.

Direct stimulation and SSEPs performed intraoperatively confirmed the accuracy of the functional imaging data. Trial periods of stimulation successfully reduced pain in three of the five patients who then underwent permanent internal placement of the system. At a mean 6-month follow up, these patients reported an average reduction in pain of 55% on a visual analog scale. The integration of functional and anatomical imaging data allows for precise and efficient surgical planning and may reduce the time necessary for intraoperative physiological verification.

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Charles Y. Liu, Brian Lee, Nicholas Boulis and Ali R. Rezai

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James K. C. Liu, Hesham Soliman, Andre Machado, Milind Deogaonkar and Ali R. Rezai

Object

Many previous studies have shown that placement of deep brain stimulation (DBS) electrodes carries a considerable risk of hemorrhage. To date, no studies have evaluated the incidence of intracranial hemorrhage after removal of DBS electrodes. The authors performed a retrospective chart review to identify the incidence and trends in hemorrhage after DBS electrode removal.

Methods

A retrospective chart review of all DBS electrodes removed at the Cleveland Clinic between October 2000 and May 2010 was performed. All patients underwent postoperative CT scanning. Each patient was evaluated for age, sex, side of placement, target, duration of lead placement, reason for removal, and medical comorbidities.

Results

A total of 78 lead removals were performed in the 10-year period (1300 leads were implanted during the same period). Of the 78 leads removed, 10 (12.8%) resulted in hemorrhages seen on postoperative CT scans. The hemorrhages were superficial cortical in 6 cases of lead removal (60%) and deep in 4 cases (40%). No statistically significant correlation to any of the factors evaluated was found. All hemorrhages were asymptomatic. The authors' retrospective study of 78 DBS lead removals revealed a high risk of intracranial hemorrhage (12.8% per lead). The risk of hemorrhage during removal is significantly greater than the risk of hemorrhage during implantation (2.0% per lead at the authors' center during the same period). There were more superficial hemorrhages, and all hemorrhages were asymptomatic.

Conclusions

Removal of DBS leads carries a significantly higher risk of postoperative hemorrhages that are seen on images but are not clinically symptomatic.

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Joshua M. Rosenow, Michael Stanton-Hicks, Ali R. Rezai and Jaimie M. Henderson

Object

Epidural spinal cord stimulation (SCS) is effective at treating refractory pain. The failure modes of the implanted hardware, however, have not been well studied. A better understanding of this could aid in improving the current procedure or designing future devices.

Methods

The authors reviewed electronic charts and operative reports of 289 patients who had undergone SCS implantation between 1998 and 2002 at the Cleveland Clinic Foundation. Data were collected on demographics, type of hardware, date of implantation procedure, indication for treatment, time to failure, and failure mode. Data were then analyzed to identify significant differences.

A total of 577 procedures were performed, 43.5% of which involved revision or removal of SCS hardware. The most common indication was complex regional pain syndrome 1, and this was followed by failed–back surgery syndrome. The median number of procedures per patient was two. Approximately 80% of all leads were the percutaneous type. The majority (62%) of leads were placed in the thoracic region, and 33.5% of all leads required revision. Poor pain relief coverage was the most common indication for revision. Surgically implanted leads broke twice as often as percutaneous leads. In 46% of the patients, hardware revision was required, and multiple revisions were necessary in 22.5%. Three-way ANOVA revealed significant differences in failure mode rates according to location (cervical compared with thoracic, p = 0.037) and failure modes (p = 0.019). Laminotomy leads tended to break and migrate sooner than percutaneous leads. Thoracic leads became infected sooner than cervical leads.

Conclusions

The results of this analysis of SCS hardware failures may be used as a basis for refining surgical technique and designing the next generation of SCS hardware.

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Mark Lee, Ali R. Rezai, Rick Abbott, Daniel H. Coelho and Fred J. Epstein

✓ Spinal cord lipomas are rare lesions, accounting for approximately 1% of all spinal cord tumors. True intramedullary spinal cord lipomas are extremely rare and are represented in the literature as scattered, single case reports. The authors present a series of six patients with intramedullary spinal cord lipomas managed at our institution from July, 1985 to July, 1993. The patients' ages ranged from 8 to 45 years. Four patients presented with newly diagnosed tumors and two had undergone previous surgery. Patients usually presented with long histories of disability followed by rapid progression of their symptoms. Most patients were in poor neurological condition on presentation. Presenting symptoms included spinal pain, dysesthetic sensory changes, gait difficulties, weakness, and incontinence. Three patients had cervical tumors, two had cervicothoracic tumors, and one patient had a thoracic tumor. Diagnostic studies, including magnetic resonance imaging, were obtained in all patients. No patient exhibited any form of spinal dysraphism or had a dural defect. All patients underwent decompressive, subtotal resections of 40% to 70% of their lesions. Follow-up times ranged from 12 to 96 months. All patients had resolution of their pain, but they generally showed no neurological improvement. As of their most recent follow-up visit, none of the patients was neurologically normal; three can function independently, although with neurological deficits. The other three patients cannot function independently and have severe neurological deficits. The authors conclude that patients with intramedullary spinal cord lipoma who present with significant neurological compromise have a very poor prognosis with regard to neurological function and generally show no improvement with surgical resection.

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Ali R. Rezai, Henry H. Woo, Mark Lee, Henry Cohen, David Zagzag and Fred J. Epstein

✓ Ependymomas are rare central nervous system (CNS) neoplasms that occasionally disseminate along the neuraxis or to extraneural sites. Definitive criteria predictive of dissemination have yet to be determined. One hundred forty patients with CNS ependymoma (88 primary spinal and 52 primary intracranial tumors) were surgically treated by the senior author (F.J.E.) between 1986 and 1994. Sixteen patients (11.4%) demonstrated tumor dissemination. The disseminated group consisted of 11 (12.5%) of 88 primary spinal and five (9.6%) of 52 primary intracranial ependymomas. The authors retrospectively reviewed the patients with CNS ependymoma and have identified several characteristics associated with dissemination from the primary tumor site. The mean time from diagnosis to dissemination was 6.8 years. The patients with disseminated disease were younger (16.8 vs. 28.3 years old, p = 0.02), had fewer gross-total resections (29% vs. 68%, p = 0.015), and had tumors with higher proliferative indices (MIB-1 staining, 13.14% vs. 2.06%, p = 0.02). High-grade tumors had a mean proliferation index of 21%, versus 2.4% and 1.6% for myxopapillary and low-grade tumors, respectively (p = 0.0003). In contrast to previous studies, tumor histology was the most significant variable for time to dissemination as determined by multivariate analysis (p = 0.008). Myxopapillary and high-grade tumors were 3.6 and 5.6 times more likely to have a shorter time to dissemination than low-grade tumors. In addition, dissemination is associated with a worse prognosis. At follow-up review, 31% of patients with disseminated disease had died compared to 7% of patients without dissemination (p = 0.04). It is concluded that younger patients with subtotal resections, myxopapillary or high-grade histology, and tumors with high proliferative indices are at substantial risk for the development of disseminated disease during their clinical course.

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Alon Y. Mogilner, Djordje Sterio, Ali R. Rezai, Martin Zonenshayn, Patrick J. Kelly and Aleksandar Beric

Object. A substantial number of patients with Parkinson disease (PD) who have undergone unilateral stereotactic pallidotomy ultimately develop symptom progression, becoming potential candidates for further surgical treatment. Bilateral subthalamic nucleus (STN) deep brain stimulation (DBS) has been shown to be effective in the treatment of a subset of patients with refractory PD. Microelectrode recording is performed to help localize the STN and guide final placement of the electrode. Potential alterations in physiological features of the STN after pallidotomy may complicate localization of this structure in this group of patients.

Methods. Bilateral STN DBS surgery guided by microelectrode recording was performed in six patients who had undergone previous unilateral pallidotomies. Physiologically obtained parameters of the STN, including trajectory length, mean firing rate, cell number, and cell density were calculated. These data were compared with those from the side without prior pallidotomy within each patient, as well as with those from our series of 49 subthalamic nuclei explored in 26 patients who had not undergone prior pallidotomy but who underwent bilateral STN stimulator placement.

In all patients, analysis of STN cellular activity on the side ipsilateral to the pallidotomy demonstrated a lower mean firing frequency than on the contralateral, intact side. The physiological features on the intact side were not significantly different from those found in our series of patients who had not undergone prior pallidotomy.

Conclusions. Physicians who perform STN surgery in patients with prior pallidotomy should be aware of the electrophysiological differences between the STN that had undergone pallidotomy and the one that had not, to avoid prolonging recording time to search for the typical STN. The implications of these findings for the current models of information processing in the basal ganglia are discussed.

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Ali R. Rezai, Andres M. Lozano, Adrian P. Crawley, Michael L. G. Joy, Karen D. Davis, Chun L. Kwan, Jonathan O. Dostrovsky, Ronald R. Tasker and David J. Mikulis

The utility of functional magnetic resonance (fMR) imaging in patients with implanted thalamic electrodes has not yet been determined. The aim of this study was to establish the safety of performing fMR imaging in patients with thalamic deep brain stimulators and to determine the value of fMR imaging in detecting cortical and subcortical activity during stimulation.

Functional MR imaging was performed in three patients suffering from chronic pain and two patients with essential tremor. Two of the three patients with pain had undergone electrode implantation in the thalamic sensory ventralis caudalis (Vc) nucleus and the other had undergone electrode implantation in both the Vc and the periventricular gray (PVG) matter. Patients with tremor underwent electrode implantation in the ventralis intermedius (Vim) nucleus. Functional MR imaging was performed during stimulation by using a pulse generator connected to a transcutaneous extension lead. Clinically, Vc stimulation evoked paresthesias in the contralateral body, PVG stimulation evoked a sensation of diffuse internal body warmth, and Vim stimulation caused tremor arrest.

Functional images were acquired using a 1.5-tesla MR imaging system. The Vc stimulation at intensities provoking paresthesias resulted in activation of the primary somatosensory cortex (SI). Stimulation at subthreshold intensities failed to activate the SI. Additional stimulation-coupled activation was observed in the thalamus, the secondary somatosensory cortex (SII), and the insula. In contrast, stimulation of the PVG electrode did not evoke paresthesias or activate the SI, but resulted in medial thalamic and cingulate cortex activation. Stimulation in the Vim resulted in thalamic, basal ganglia, and SI activation.

An evaluation of the safety of the procedure indicated that significant current could be induced within the electrode if a faulty connecting cable (defective insulation) came in contact with the patient. Simple precautions, such as inspection of wires for fraying and prevention of their contact with the patient, enabled the procedure to be conducted safely. Clinical safety was further corroborated by performing 86 MR studies in patients in whom electrodes had been implanted with no adverse clinical effects.

This is the first report of the use of fMR imaging during stimulation with implanted thalamic electrodes. The authors' findings demonstrate that fMR imaging can safely detect the activation of cortical and subcortical neuronal pathways during stimulation and that stimulation does not interfere with imaging. This approach offers great potential for understanding the mechanisms of action of deep brain stimulation and those underlying pain and tremor generation.

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Ali R. Rezai, Andres M. Lozano, Adrian P. Crawley, Michael L. G. Joy, Karen D. Davis, Chun L. Kwan, Jonathan O. Dostrovsky, Ronald R. Tasker and David J. Mikulis

✓ The utility of functional magnetic resonance (fMR) imaging in patients with implanted thalamic electrodes has not yet been determined. The aim of this study was to establish the safety of performing fMR imaging in patients with thalamic deep brain stimulators and to determine the value of fMR imaging in detecting cortical and subcortical activity during stimulation.

Functional MR imaging was performed in three patients suffering from chronic pain and two patients with essential tremor. Two of the three patients with pain had undergone electrode implantation in the thalamic sensory ventralis caudalis (Vc) nucleus and the other had undergone electrode implantation in both the Vc and the periventricular gray (PVG) matter. Patients with tremor underwent electrode implantation in the ventralis intermedius (Vim) nucleus. Functional MR imaging was performed during stimulation by using a pulse generator connected to a transcutaneous extension lead. Clinically, Vc stimulation evoked paresthesias in the contralateral body, PVG stimulation evoked a sensation of diffuse internal body warmth, and Vim stimulation caused tremor arrest.

Functional images were acquired using a 1.5-tesla MR imaging system. The Vc stimulation at intensities provoking paresthesias resulted in activation of the primary somatosensory cortex (SI). Stimulation at subthreshold intensities failed to activate the SI. Additional stimulation-coupled activation was observed in the thalamus, the secondary somatosensory cortex (SII), and the insula. In contrast, stimulation of the PVG electrode did not evoke paresthesias or activate the SI, but resulted in medial thalamic and cingulate cortex activation. Stimulation in the Vim resulted in thalamic, basal ganglia, and SI activation.

An evaluation of the safety of the procedure indicated that significant current could be induced within the electrode if a faulty connecting cable (defective insulation) came in contact with the patient. Simple precautions, such as inspection of wires for fraying and prevention of their contact with the patient, enabled the procedure to be conducted safely. Clinical safety was further corroborated by performing 86 MR studies in patients in whom electrodes had been implanted with no adverse clinical effects.

This is the first report of the use of fMR imaging during stimulation with implanted thalamic electrodes. The authors' findings demonstrate that fMR imaging can safely detect the activation of cortical and subcortical neuronal pathways during stimulation and that stimulation does not interfere with imaging. This approach offers great potential for understanding the mechanisms of action of deep brain stimulation and those underlying pain and tremor generation.

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Scott L. Rauch, Darin D. Dougherty, Donald Malone, Ali Rezai, Gerhard Friehs, Alan J. Fischman, Nathaniel M. Alpert, Suzanne N. Haber, Paul H. Stypulkowski, Mark T. Rise, Steven A. Rasmussen and Benjamin D. Greenberg

Object

Deep brain stimulation (DBS) of the ventral [anterior internal] capsule/ventral striatum (VC/VS) is under investigation as an alternative to anterior capsulotomy for severe obsessive–compulsive disorder (OCD). In neuroimaging studies of patients with OCD, dysfunction in the orbitofrontal and anterior cingulate cortex, striatum, and thalamus has been identified; and modulation of activity in this circuit has been observed following successful nonsurgical treatment. The purpose of the current study was to test hypotheses regarding changes in regional cerebral blood flow (rCBF) during acute DBS at the VC/VS target in patients with OCD who were participating in a clinical DBS trial.

Methods

Six patients enrolled in a DBS trial for OCD underwent positron emission tomography to measure rCBF; the rCBF measured during acute DBS at high frequency was then compared with those measured during DBS at low frequency and off (control) conditions. On the basis of neuroanatomical knowledge about the VC/VS and neuroimaging data on OCD, the authors predicted that acute DBS at this target would result in modulation of activity within the implicated frontal–basal ganglia–thalamic circuit. Data were analyzed using statistical parametric mapping.

In a comparison of acute high-frequency DBS with control conditions, the authors found significant activation of the orbitofrontal cortex, anterior cingulate cortex, striatum, globus pallidus, and thalamus.

Conclusions

Acute DBS at the VC/VS target is associated with activation of the circuitry implicated in OCD. Further studies will be necessary to replicate these findings and to determine the neural effects associated with chronic VC/VS DBS. Moreover, additional data are needed to investigate whether pretreatment imaging profiles can be used to predict a patient’s subsequent clinical response to chronic DBS.