Epilepsy Research (2014) 108, 547—554
journal homepage: www.elsevier.com/locate/epilepsyres
Stereotactic laser ablation of epileptogenic periventricular nodular heterotopia Yoshua Esquenazi a, Giridhar P. Kalamangalam b, Jeremy D. Slater b, Robert C. Knowlton b, Elliott Friedman c, Saint-Aaron Morris a, Anil Shetty d, Ashok Gowda d, Nitin Tandon a,e,∗ a
Vivian L. Smith Department of Neurosurgery, University of Texas Health Science Center at Houston, Medical School, Houston, TX, USA b Department of Neurology, University of Texas Health Science Center at Houston, Medical School, Houston, TX, USA c Department of Diagnostic and Interventional Imaging, University of Texas Health Science Center at Houston, Medical School, Houston, TX, USA d Visualase Inc., Houston, TX, USA e Mischer Neuroscience Institute, Memorial Hermann Hospital, Texas Medical Center, USA Received 11 September 2013; received in revised form 9 December 2013; accepted 14 January 2014 Available online 30 January 2014
KEYWORDS Cortical dysplasia periventricular nodular heterotopia; Medically refractory epilepsy; Epilepsy surgery; Thermal therapy; MRI guided laser ablation
Summary Periventricular nodular heterotopia (PVNH) is a neuronal migrational disorder often associated with pharmacoresistant epilepsy (PRE). Resective surgery for PVNH is limited by its deep location, and the overlying eloquent cortex or white matter. Stereotactic MR guided laser interstitial thermal therapy (MRgLITT) has recently become available for controlled focal ablation, enabling us to target these lesions. We here demonstrate the novel application and techniques for the use of MRgLITT in the management of PVNH epilepsy. Comprehensive presurgical evaluation, including intracranial EEG monitoring in two patients revealed the PVNH to be crucially involved in their PRE. We used MRgLITT to maximally ablate the PVNH in both cases. In the first case, seizure medication adjustment coupled with PVNH ablation, and in the second, PVNH ablation in addition to temporal lobectomy rendered the patient seizure free. A transient visual deficit occurred following ablation in the second patient. MRgLITT is a promising minimally invasive technique for ablation of epileptogenic PVNH, a disease not generally viewed as surgically treatable epilepsy. We also show here the feasibility of applying this technique through multiple trajectories and to create lesions of complex shapes. The broad applicability and long term efficacy of MRgLITT need to be elaborated further. © 2014 Elsevier B.V. All rights reserved.
∗
Corresponding author at: Vivian L. Smith Department of Neurosurgery, The University of Texas Health Science Center at Houston, Medical School, 6400 Fannin # 2800, Houston, TX 77030, USA. Tel.: +1 713 704 7100. E-mail address: [email protected] (N. Tandon). 0920-1211/$ — see front matter © 2014 Elsevier B.V. All rights reserved. http://dx.doi.org/10.1016/j.eplepsyres.2014.01.009
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Introduction
Patient 1
Periventricular nodular heterotopia (PVNH) is a neuronal migration disorder characterized by subependymal gray matter nodules that fail to migrate from the periventricular germinal matrix. These nodules range in size from small, discrete neuronal clusters to large multinodular conglomerates, which along with a broader region of cortical dysplasia can result in severe focal drug resistant epilepsy (Battaglia et al., 2006; d’Orsi et al., 2004). The deep location, and the large extent of these lesions along the ventricle walls render resective surgical strategies difficult. This is especially true in cases where eloquent cortical or critical white matter tracts surround these lesions. Minimally invasive approaches for the management of PVNH thus far include stereotactically guided radiofrequency lesions (Schmitt et al., 2011), thermo-coagulation (Catenoix et al., 2008; Guenot et al., 2004) and radiosurgery (Sarkar et al., 2011). None of these therapeutic options, however, provide any measure of real time monitoring of the therapy, diminishing the margin of safety and their potential application. This introduction of the recently FDA approved, stereotactic MR guided laser interstitial thermal therapy (MRgLITT), that incorporates real time thermal monitoring of the ablation process and feedback control over the laser energy delivery, provides new approach to treat these lesions. Here we report on the first two cases of PVNH patients ever treated with this novel technique and their short term outcomes.
The first patient was a 48 year-old right-handed female with a 24 year history of intractable epilepsy. She had complex partial seizures typically twice a month, preceded by an aura of tunnel vision. Trials of six different antiepileptic drugs (AEDs) failed to control her seizures. Evaluation with scalp video-EEG monitoring suggested left frontal onset seizures based on semiology characterized by right head and torso version, flexion of the right arm and clenching of the fist lasting about 10—30 s; they were not well localized by EEG. MRI revealed the presence of a left PVNH surrounding the ependyma of the left frontal horn (Fig. 1). Her brain 2[18 F]fluoro-2-deoxy-D-glucose positron emission tomography (FDG-PET) scan showed mild relative hypometabolism in the right superior postcentral gyrus. Neuropsychological testing revealed a full scale IQ of 93, Verbal IQ of 108 and a performance IQ of 81. She was found to have deficient verbal fluency for phonemic exemplars, deficient memory for spatial positions, and borderline deficient spatial memory. In summary, the findings were believed to reflect left frontal and right mesial temporal lobe dysfunction. To delineate the ictal onset zone precisely, a small left frontal craniotomy was performed for subdural strip placement as well as placement of two depth electrodes into the PVNH (Fig. 1). Strip electrodes were placed over the anterior, lateral, posterior and mesial fontal regions. Interictal spikes were recorded over the posterior/superior frontal region. Three complex partial seizures were recorded that originated from the posterior superior frontal region with concurrent involvement and prolongation of ictal activity in the PVNH. Given the location of the neocortical onsets over eloquent cortex in the posterior dominant frontal lobe, a decision was made to first attempt thermal ablation of the left frontal heterotopic gray matter.
Methods Informed consent was obtained following study approval by our institution’s committee for protection of human subjects to be able to collect and report these data. Both subjects underwent initial scalp video EEG, imaging and neuropsychological testing as per protocol at the UT Epilepsy Surgery Program. The cases were discussed at a multidisciplinary epilepsy patient management conference that recommended each of the surgical interventions. Specific patient details are described below:
Patient 2 The second patient was a 25 year-old right handed male with pharmacoresistant complex partial seizures since age 23. His recurrent habitual seizures occurred 1—2 times/day, increasing in frequency and severity over the past year. They
Figure 1 (Patient 1) Preoperative axial (A), and coronal (B and C) T2-MRI. Arrows point to the left frontal PVNH (A and B) and one of the depth electrodes (C) along the PVNH.
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Figure 2 (Patient 2) Coronal and axial FDG-PET (A, B and C, D) demonstrating markedly decreased activity in the left temporal lobe. Coronal T2-MRI (E and F) arrows demonstrate the PVNH in the temporal—occipital region. Axial post contrast MRI demonstrates placement of the depth electrodes along the length of the hippocampus (G) and the PVNH (H).
were comprised of déjà vu as an aura followed by loss of awareness, then inert motor behavior with only oral and manual automatisms. Rarely his seizures secondarily generalized. Scalp video EEG monitoring confirmed a left temporal lobe electroclinical syndrome with temporal interictal discharges and ictal onsets. MRI of the brain (Fig. 2) revealed bilateral PVNH adjacent to the ventricular wall of the temporal horns extending to the atria of the lateral ventricles, structurally normal hippocampi bilaterally and anterior left temporal lobe volume loss. FDG PET imaging showed evidence of moderately decreased metabolic activity throughout the left temporal lobe, including the hippocampus (Fig. 2) Neuropsychological evaluation revealed a full scale IQ of 95, verbal IQ of 85, and performance IQ of 107, and suggested left fronto-temporal dysfunction. Given intact hippocampal structure, an intracarotid amytal (Wada) procedure was performed (Breier et al., 1999), revealing left hemisphere lateralization of language with intact memory function (8/8) bilaterally. To localize the ictal onset zone and to discriminate between hippocampal and PVNH onset of the seizures, an intracranial evaluation with depth and strip electrodes was carried out. Three depth electrodes were placed orthogonal to the middle temporal gyrus with destinations in the anterior, middle and posterior portions of the left PVNH. One depth electrode was placed in the amygdala and two in the hippocampus (head and body) (Fig. 2). Four strip electrodes were placed through a single temporal burr hole and directed to the temporal pole, lateral temporal, sub-temporal and lateral frontal. Interictal epileptiform discharges were observed independently from both the mesial temporal lobe and the PVNH. A total of 7 seizures were recorded during the intracranial evaluation. In 4 seizures, the initial ictal patterns were localized wholly within the PVNH tissue, with secondary spread to mesial temporal structures and overlying temporal
neocortex. A single clinical seizure originated independently from the left mesial temporal lobe and two subclinical seizures originated independently from the left posterior temporal neocortex, in the vicinity of Wernicke’s area. A clinical decision was made to proceed with stereotactic ablation of the PVNH in to address the predominant seizure onset zone in an effort to avoid a larger resection and the potential for memory loss resulting from surgery.
MR-guided laser ablation technique Under general anesthesia an MR compatible stereotactic head frame (Leksell) was placed and scans obtained using a 3.0T MRI (General Electric Signa EXCITE) with standard quadrature head coil. A stereotactic planning workstation (Framelink Cranial Stealth navigation system — Medtronic Boulder, CO, USA) was used to design trajectories to allow maximal traversal of the PVNH. In the operating room, the laser probe with cooling catheter (Visualase, Inc., Houston, TX) was placed at the target using a 3.2 mm twist drill hole and through a polycarbonate anchor bolt that held the probe in place after the Leksell frame was removed. Back in the MRI scanner, T2 weighted fluid-attenuated inversion recovery (FLAIR) images were acquired to confirm precise placement. Two oblique views, orthogonal to each other and containing full length views of the probe were used to monitor the ablation. MR thermal imaging was accomplished using a fast gradient echo (SPGR) sequence (FOV 24 cm × 24 cm; acquisition matrix, 256 × 120; echo time, 20 ms; repetition time, 45 ms; flip angle, 30◦ ; band width, 12.6 kHz), which required 5 s for a single acquisition and which was run repeatedly during the therapy (Figs. 3 and 4). The MR guided laser interstitial thermal therapy (MRgLITT) comprises of a computer workstation, a 15 W 980 nm diode laser, a cooling pump, and the disposable
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Figure 3 (Patient 1) Laser ablation procedure in patient 1: (A) placement of the probe, arrow demonstrates the (PVNH) target. (B) Treatment temperature map, and (C) damage estimate. (D) Post-ablation contrast MRI, arrow demonstrates the post-ablation zone. Real-time monitoring of temperature and damage estimate enabled controlled ablation of PVNH. 1 slice orthogonal monitoring is demonstrated.
laser applicator probe (400 m core silica fiber-optic cable with a cylindrical diffusing tip) housed within a 1.65 mm diameter saline-cooled polycarbonate catheter (McNichols et al., 2004). An ethernet connection between the workstation and the scanner was used to retrieve reconstructed images. Extracted thermal data were used to produce colorcoded ‘‘thermal’’ and estimate ‘‘damage’’ images based on an Arrhenius rate process model and displayed on the workstation. A damage image accounting for the cumulative effects of the time-temperature history of each voxel in the image was generated for each ablation site. In addition to this visualization, prescribed ‘‘limit temperatures’’ were placed at specific points on the image, to prevent injury to these regions, by automatically deactivating the laser, if during the treatment, the computed temperature at these targets exceeded the associated limit temperature.
Specific details of MRgLITT for each case In both patients, low power test pulses were initially applied (3—4 W, 15—45 s) to verify thermal coverage. The applicator was adjusted by repositioning the fiberoptic diffuser along the length of the cooling catheter to refine coverage. Subsequently, treatment doses were applied along the length of this cooling catheter — thereby producing an ellipsoidal ablation zone, to match the shape of the PVNH. In Patient 1, a single entry point was made in the frontal area (Fig. 3). Critical safety points were placed at the edge of the caudate nucleus and adjoining the presumed location of the corticospinal tract to limit temperatures there to below 50 ◦ C. Monitoring was done in a single oblique slice along the length of the fiber. In Patient 2, the PVNH was complex in shape and voluminous. Therefore, two trajectories
Figure 4 (Patient 2) (A) Patient with the Leksell frame attached in the sitting position. Parieto—occipital (1) and occipital probes (2) are entering the skull. (B) Arrows point to the PVNH, probes 1 and 2 are demonstrated. (C and E) Treatment temperature map. (D and F) Irreversible damage estimate. (G and H) Post-contrast imaging to confirm extent of ablation.
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Figure 5 (Patient 1): (A) Post ablation (3-month) FLAIR axial MRI and (B) T-1 post-contrast coronal MRI, demonstrating the ablation area along the frontal PVNH.
— one parieto-occipital (target 1) and one temporooccipital (target 2), were utilized to target it and to use the two ablations along these tracts to maximally target the abnormality. Safety zones were placed along the presumptive location of the geniculocalcarine fibers. In this patient, real time temperature monitoring was done in 2 orthogonal slices — oblique axial and oblique sagittal (Fig. 4). Fiber 1 required one pullback and fiber 2 required three pullbacks to maximize coverage of the PVNH. After completion of the ablation procedure, post ablation T1 weighted plus gadolinium contrast series were acquired to visualize the actual extent of the ablation zone (Tracz et al., 1993) (Figs. 3 and 4).
Results In both patients, the placement of the probes was accurate and the thermal ablation cycles were successfully accomplished (Figs. 5 and 6). In the first patient, the ablation cylindroid was 24 mm long and 9 mm wide and damage maps as well as post contrast MR imaging showed the damage to be contoured along the ventricular wall (Fig. 5). In the second case the damage estimate measured 27 × 25 × 12 for fiber 1 and 50 mm × 13 mm × 15 mm for fiber 2. Post contrast imaging confirmed the contiguous ablation area as a result of the precise placement of the two laser catheters and effective coverage of the heterotopia (Fig. 6). The
patient tolerated the procedure well, but developed a complete right homonymous hemianopsia post-operatively that responded to administration of steroids to become an inferior temporal quadrantanopsia by 2 weeks and improved further by 6 weeks. Both patients were discharged home on post-operative day #1.
Seizure outcomes Patient 1 Following ablation the patient remained completely seizure free for one month. Her seizures then recurred, and by the time of her 3 months follow up the frequency was back to her baseline. With a change back to one of her prior medications (that had produced the best improvement but never total control prior to surgery), she again became seizure free (now at twelve months). Patient 2 Following ablation, the patient remained seizure free for 12 weeks. Seizures however recurred and were identical to those pre ablation. A repeat scalp video-EEG study showed interictal left temporal slowing and sharp waves, and left temporal onset seizures. Repeat MRI of the brain showed postoperative changes related to the ablation of the left PVNH. The patient underwent a craniotomy and intracranial
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Figure 6 (Patient 2): (A) T-2 coronal MRI prior to ablation, arrows show bilateral temporal—occipital PVNH. (B) Post ablation (3-month) T-2 coronal MRI, arrows show ablation along the two used trajectories.
electrode placement seven months post-ablation. Multiple strips and grids were placed to cover a wide cortical area over the frontal and temporal region, and a depth electrode was placed in the hippocampus. This evaluation demonstrated multiple interictal and ictal discharges arising chiefly from the mesial temporal lobe, as well as the temporal neocortex; there was no evidence of seizure activity from the area around the prior location of the PVNH. The patient underwent an anterior temporal lobectomy and amygdalohippocampectomy. He has remained seizure free for nine months following resection.
Discussion MR guided laser ablation has previously been employed in neurooncology, with good outcomes and acceptable safety profiles (Ascher et al., 1991; Kahn et al., 1994; Kettenbach et al., 1998). The Visualase system is the first MR guided laser ablation system approved by the FDA for soft tissue ablation in neurosurgery. Its safety has been demonstrated with the ablation of treatment resistant focal metastatic brain tumors and recurrent glioblastoma (Carpentier et al., 2012, 2011). More recently the use of this system for thermal destruction of epileptic foci in children (hypothalamic hamartoma, cortical dysplasia, tuberous sclerosis nodules) has shown promising results (Curry et al., 2012). Prior minimally invasive approaches for the management of PVNH have included stereotactic guided radiofrequency lesioning, (Schmitt et al., 2011) thermocoagulation (Catenoix et al., 2008; Guenot et al., 2004) and stereotactic radiosurgery (Sarkar et al., 2011). In this report, we present the first application of MRgLITT for the management of patients with PVNH associated epilepsy and demonstrate favorable outcomes in both patients. In the second patient, the results of the initial invasive video EEG
recordings revealed evidence of seizures originating from both the PVNH as well as the medial temporal structures. As previously seen in studies using intracranial EEG recordings from patients with PVNH, the seizure onset zone in these cases is rather broad, and better viewed as a network. Ablation of the presumed critical node (the PVNH) in this network may or may not ensure seizure control, (Aghakhani et al., 2005; Dubeau et al., 1995; Kothare et al., 1998) implying the existence of a widespread epileptogenic zone, (Kitaura et al., 2012; Li et al., 1997; Valton et al., 2008) and an existing ‘‘functional’’ relationship between the nodule and the overlying cortex (Tassi et al., 2005). The latter was the source of the second patient’s post ablation seizures that eventually prompted a standard temporal lobectomy with amygdalohippocampectomy. In this patient, due to the complex shape and large volume of the PVNH, we decided to use two separate ablation catheters to create the appropriately sized and shaped ablation zone. The advantage of using multiple probes for the ablation process enables the use of this technology for irregularly shaped, multiple, and complex lesions than might be accomplished otherwise. Additionally the implementation of the ablation process can be performed in a single or in staged procedures. We believe that in this patient the ablation of the PVNH was crucial for his seizure freedom since the predominance of seizure activity originated within PVNH tissue. In a phase II evaluation following MRgLITT no further seizures were recorded from depth electrodes placed in the small residual PVNH and seizures arose exclusively from the mesial temporal lobe and temporal neocortex. While we cannot know for certainty if a temporal lobectomy and amygdalohippocampectomy prior to the ablation of the PVNH would have rendered the patient seizure free, this is unlikely due to the patient’s ictal patterns in the first intracranial evaluation, that originated predominantly and clearly in the PVNH.
Stereotactic laser ablation Our view was that ablation of the PVNH using this minimally invasive approach would be worth trying prior to undergoing a more extensive resection, as it had atleast a modest chance of improving the clinical outcome in this patient with a epileptic network that involved structures crucial to memory and language. MRgLITT enabled us to target components of the epileptogenic network that are generally not amenable to microsurgical intervention. The PVNH tissue is located deep, and in both of these cases, was overlaid by eloquent cortex and by crucial white matter tracts. A traditional resective surgery would therefore have resulted in the disruption of normal uninvolved brain. The ability to monitor and enable closed loop control of the ablation in realtime maximizes the safety of this technique, as compared with other minimally invasive approaches. The incorporation of tractography data into planning and the ablation in the future might prevent inadvertent compromise of white matter fibers. Finally, the procedure is extremely well tolerated, with a very short period of hospitalization, and reduced costs. Moreover, its use does not preclude or make more challenging subsequent resections in cases of failure of seizure control or seizure recurrence. The experience presented in this study with MRgLITT in two patients with epilepsy secondary to PVNH is admittedly limited, in part to the rarity of patients suffering from epilepsy related to PVNH as well as the novelty of the technology. To the best of our knowledge, there are only 4 previously published cases in which PVNHs were tackled with minimally invasive approaches. Furthermore, it is unlikely that our results of relative seizure control in the absence of permanent neurological deficits could have been accomplished without the use of MRgLITT technology.
Conclusion MRgLITT possesses significant potential as a minimally invasive technique for ablation of PVNH, and more generally, as an adjunct in the surgical management of lesional epilepsy. In this study we demonstrate the safety, feasibility and limited efficacy of MRgLITT in PVNH-associated epilepsy, though its long-term efficacy will be revealed as more centers adopt the technology in the future.
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journal homepage: www.elsevier.com/locate/epilepsyres
Stereotactic laser ablation of epileptogenic periventricular nodular heterotopia Yoshua Esquenazi a, Giridhar P. Kalamangalam b, Jeremy D. Slater b, Robert C. Knowlton b, Elliott Friedman c, Saint-Aaron Morris a, Anil Shetty d, Ashok Gowda d, Nitin Tandon a,e,∗ a
Vivian L. Smith Department of Neurosurgery, University of Texas Health Science Center at Houston, Medical School, Houston, TX, USA b Department of Neurology, University of Texas Health Science Center at Houston, Medical School, Houston, TX, USA c Department of Diagnostic and Interventional Imaging, University of Texas Health Science Center at Houston, Medical School, Houston, TX, USA d Visualase Inc., Houston, TX, USA e Mischer Neuroscience Institute, Memorial Hermann Hospital, Texas Medical Center, USA Received 11 September 2013; received in revised form 9 December 2013; accepted 14 January 2014 Available online 30 January 2014
KEYWORDS Cortical dysplasia periventricular nodular heterotopia; Medically refractory epilepsy; Epilepsy surgery; Thermal therapy; MRI guided laser ablation
Summary Periventricular nodular heterotopia (PVNH) is a neuronal migrational disorder often associated with pharmacoresistant epilepsy (PRE). Resective surgery for PVNH is limited by its deep location, and the overlying eloquent cortex or white matter. Stereotactic MR guided laser interstitial thermal therapy (MRgLITT) has recently become available for controlled focal ablation, enabling us to target these lesions. We here demonstrate the novel application and techniques for the use of MRgLITT in the management of PVNH epilepsy. Comprehensive presurgical evaluation, including intracranial EEG monitoring in two patients revealed the PVNH to be crucially involved in their PRE. We used MRgLITT to maximally ablate the PVNH in both cases. In the first case, seizure medication adjustment coupled with PVNH ablation, and in the second, PVNH ablation in addition to temporal lobectomy rendered the patient seizure free. A transient visual deficit occurred following ablation in the second patient. MRgLITT is a promising minimally invasive technique for ablation of epileptogenic PVNH, a disease not generally viewed as surgically treatable epilepsy. We also show here the feasibility of applying this technique through multiple trajectories and to create lesions of complex shapes. The broad applicability and long term efficacy of MRgLITT need to be elaborated further. © 2014 Elsevier B.V. All rights reserved.
∗
Corresponding author at: Vivian L. Smith Department of Neurosurgery, The University of Texas Health Science Center at Houston, Medical School, 6400 Fannin # 2800, Houston, TX 77030, USA. Tel.: +1 713 704 7100. E-mail address: [email protected] (N. Tandon). 0920-1211/$ — see front matter © 2014 Elsevier B.V. All rights reserved. http://dx.doi.org/10.1016/j.eplepsyres.2014.01.009
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Introduction
Patient 1
Periventricular nodular heterotopia (PVNH) is a neuronal migration disorder characterized by subependymal gray matter nodules that fail to migrate from the periventricular germinal matrix. These nodules range in size from small, discrete neuronal clusters to large multinodular conglomerates, which along with a broader region of cortical dysplasia can result in severe focal drug resistant epilepsy (Battaglia et al., 2006; d’Orsi et al., 2004). The deep location, and the large extent of these lesions along the ventricle walls render resective surgical strategies difficult. This is especially true in cases where eloquent cortical or critical white matter tracts surround these lesions. Minimally invasive approaches for the management of PVNH thus far include stereotactically guided radiofrequency lesions (Schmitt et al., 2011), thermo-coagulation (Catenoix et al., 2008; Guenot et al., 2004) and radiosurgery (Sarkar et al., 2011). None of these therapeutic options, however, provide any measure of real time monitoring of the therapy, diminishing the margin of safety and their potential application. This introduction of the recently FDA approved, stereotactic MR guided laser interstitial thermal therapy (MRgLITT), that incorporates real time thermal monitoring of the ablation process and feedback control over the laser energy delivery, provides new approach to treat these lesions. Here we report on the first two cases of PVNH patients ever treated with this novel technique and their short term outcomes.
The first patient was a 48 year-old right-handed female with a 24 year history of intractable epilepsy. She had complex partial seizures typically twice a month, preceded by an aura of tunnel vision. Trials of six different antiepileptic drugs (AEDs) failed to control her seizures. Evaluation with scalp video-EEG monitoring suggested left frontal onset seizures based on semiology characterized by right head and torso version, flexion of the right arm and clenching of the fist lasting about 10—30 s; they were not well localized by EEG. MRI revealed the presence of a left PVNH surrounding the ependyma of the left frontal horn (Fig. 1). Her brain 2[18 F]fluoro-2-deoxy-D-glucose positron emission tomography (FDG-PET) scan showed mild relative hypometabolism in the right superior postcentral gyrus. Neuropsychological testing revealed a full scale IQ of 93, Verbal IQ of 108 and a performance IQ of 81. She was found to have deficient verbal fluency for phonemic exemplars, deficient memory for spatial positions, and borderline deficient spatial memory. In summary, the findings were believed to reflect left frontal and right mesial temporal lobe dysfunction. To delineate the ictal onset zone precisely, a small left frontal craniotomy was performed for subdural strip placement as well as placement of two depth electrodes into the PVNH (Fig. 1). Strip electrodes were placed over the anterior, lateral, posterior and mesial fontal regions. Interictal spikes were recorded over the posterior/superior frontal region. Three complex partial seizures were recorded that originated from the posterior superior frontal region with concurrent involvement and prolongation of ictal activity in the PVNH. Given the location of the neocortical onsets over eloquent cortex in the posterior dominant frontal lobe, a decision was made to first attempt thermal ablation of the left frontal heterotopic gray matter.
Methods Informed consent was obtained following study approval by our institution’s committee for protection of human subjects to be able to collect and report these data. Both subjects underwent initial scalp video EEG, imaging and neuropsychological testing as per protocol at the UT Epilepsy Surgery Program. The cases were discussed at a multidisciplinary epilepsy patient management conference that recommended each of the surgical interventions. Specific patient details are described below:
Patient 2 The second patient was a 25 year-old right handed male with pharmacoresistant complex partial seizures since age 23. His recurrent habitual seizures occurred 1—2 times/day, increasing in frequency and severity over the past year. They
Figure 1 (Patient 1) Preoperative axial (A), and coronal (B and C) T2-MRI. Arrows point to the left frontal PVNH (A and B) and one of the depth electrodes (C) along the PVNH.
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Figure 2 (Patient 2) Coronal and axial FDG-PET (A, B and C, D) demonstrating markedly decreased activity in the left temporal lobe. Coronal T2-MRI (E and F) arrows demonstrate the PVNH in the temporal—occipital region. Axial post contrast MRI demonstrates placement of the depth electrodes along the length of the hippocampus (G) and the PVNH (H).
were comprised of déjà vu as an aura followed by loss of awareness, then inert motor behavior with only oral and manual automatisms. Rarely his seizures secondarily generalized. Scalp video EEG monitoring confirmed a left temporal lobe electroclinical syndrome with temporal interictal discharges and ictal onsets. MRI of the brain (Fig. 2) revealed bilateral PVNH adjacent to the ventricular wall of the temporal horns extending to the atria of the lateral ventricles, structurally normal hippocampi bilaterally and anterior left temporal lobe volume loss. FDG PET imaging showed evidence of moderately decreased metabolic activity throughout the left temporal lobe, including the hippocampus (Fig. 2) Neuropsychological evaluation revealed a full scale IQ of 95, verbal IQ of 85, and performance IQ of 107, and suggested left fronto-temporal dysfunction. Given intact hippocampal structure, an intracarotid amytal (Wada) procedure was performed (Breier et al., 1999), revealing left hemisphere lateralization of language with intact memory function (8/8) bilaterally. To localize the ictal onset zone and to discriminate between hippocampal and PVNH onset of the seizures, an intracranial evaluation with depth and strip electrodes was carried out. Three depth electrodes were placed orthogonal to the middle temporal gyrus with destinations in the anterior, middle and posterior portions of the left PVNH. One depth electrode was placed in the amygdala and two in the hippocampus (head and body) (Fig. 2). Four strip electrodes were placed through a single temporal burr hole and directed to the temporal pole, lateral temporal, sub-temporal and lateral frontal. Interictal epileptiform discharges were observed independently from both the mesial temporal lobe and the PVNH. A total of 7 seizures were recorded during the intracranial evaluation. In 4 seizures, the initial ictal patterns were localized wholly within the PVNH tissue, with secondary spread to mesial temporal structures and overlying temporal
neocortex. A single clinical seizure originated independently from the left mesial temporal lobe and two subclinical seizures originated independently from the left posterior temporal neocortex, in the vicinity of Wernicke’s area. A clinical decision was made to proceed with stereotactic ablation of the PVNH in to address the predominant seizure onset zone in an effort to avoid a larger resection and the potential for memory loss resulting from surgery.
MR-guided laser ablation technique Under general anesthesia an MR compatible stereotactic head frame (Leksell) was placed and scans obtained using a 3.0T MRI (General Electric Signa EXCITE) with standard quadrature head coil. A stereotactic planning workstation (Framelink Cranial Stealth navigation system — Medtronic Boulder, CO, USA) was used to design trajectories to allow maximal traversal of the PVNH. In the operating room, the laser probe with cooling catheter (Visualase, Inc., Houston, TX) was placed at the target using a 3.2 mm twist drill hole and through a polycarbonate anchor bolt that held the probe in place after the Leksell frame was removed. Back in the MRI scanner, T2 weighted fluid-attenuated inversion recovery (FLAIR) images were acquired to confirm precise placement. Two oblique views, orthogonal to each other and containing full length views of the probe were used to monitor the ablation. MR thermal imaging was accomplished using a fast gradient echo (SPGR) sequence (FOV 24 cm × 24 cm; acquisition matrix, 256 × 120; echo time, 20 ms; repetition time, 45 ms; flip angle, 30◦ ; band width, 12.6 kHz), which required 5 s for a single acquisition and which was run repeatedly during the therapy (Figs. 3 and 4). The MR guided laser interstitial thermal therapy (MRgLITT) comprises of a computer workstation, a 15 W 980 nm diode laser, a cooling pump, and the disposable
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Figure 3 (Patient 1) Laser ablation procedure in patient 1: (A) placement of the probe, arrow demonstrates the (PVNH) target. (B) Treatment temperature map, and (C) damage estimate. (D) Post-ablation contrast MRI, arrow demonstrates the post-ablation zone. Real-time monitoring of temperature and damage estimate enabled controlled ablation of PVNH. 1 slice orthogonal monitoring is demonstrated.
laser applicator probe (400 m core silica fiber-optic cable with a cylindrical diffusing tip) housed within a 1.65 mm diameter saline-cooled polycarbonate catheter (McNichols et al., 2004). An ethernet connection between the workstation and the scanner was used to retrieve reconstructed images. Extracted thermal data were used to produce colorcoded ‘‘thermal’’ and estimate ‘‘damage’’ images based on an Arrhenius rate process model and displayed on the workstation. A damage image accounting for the cumulative effects of the time-temperature history of each voxel in the image was generated for each ablation site. In addition to this visualization, prescribed ‘‘limit temperatures’’ were placed at specific points on the image, to prevent injury to these regions, by automatically deactivating the laser, if during the treatment, the computed temperature at these targets exceeded the associated limit temperature.
Specific details of MRgLITT for each case In both patients, low power test pulses were initially applied (3—4 W, 15—45 s) to verify thermal coverage. The applicator was adjusted by repositioning the fiberoptic diffuser along the length of the cooling catheter to refine coverage. Subsequently, treatment doses were applied along the length of this cooling catheter — thereby producing an ellipsoidal ablation zone, to match the shape of the PVNH. In Patient 1, a single entry point was made in the frontal area (Fig. 3). Critical safety points were placed at the edge of the caudate nucleus and adjoining the presumed location of the corticospinal tract to limit temperatures there to below 50 ◦ C. Monitoring was done in a single oblique slice along the length of the fiber. In Patient 2, the PVNH was complex in shape and voluminous. Therefore, two trajectories
Figure 4 (Patient 2) (A) Patient with the Leksell frame attached in the sitting position. Parieto—occipital (1) and occipital probes (2) are entering the skull. (B) Arrows point to the PVNH, probes 1 and 2 are demonstrated. (C and E) Treatment temperature map. (D and F) Irreversible damage estimate. (G and H) Post-contrast imaging to confirm extent of ablation.
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Figure 5 (Patient 1): (A) Post ablation (3-month) FLAIR axial MRI and (B) T-1 post-contrast coronal MRI, demonstrating the ablation area along the frontal PVNH.
— one parieto-occipital (target 1) and one temporooccipital (target 2), were utilized to target it and to use the two ablations along these tracts to maximally target the abnormality. Safety zones were placed along the presumptive location of the geniculocalcarine fibers. In this patient, real time temperature monitoring was done in 2 orthogonal slices — oblique axial and oblique sagittal (Fig. 4). Fiber 1 required one pullback and fiber 2 required three pullbacks to maximize coverage of the PVNH. After completion of the ablation procedure, post ablation T1 weighted plus gadolinium contrast series were acquired to visualize the actual extent of the ablation zone (Tracz et al., 1993) (Figs. 3 and 4).
Results In both patients, the placement of the probes was accurate and the thermal ablation cycles were successfully accomplished (Figs. 5 and 6). In the first patient, the ablation cylindroid was 24 mm long and 9 mm wide and damage maps as well as post contrast MR imaging showed the damage to be contoured along the ventricular wall (Fig. 5). In the second case the damage estimate measured 27 × 25 × 12 for fiber 1 and 50 mm × 13 mm × 15 mm for fiber 2. Post contrast imaging confirmed the contiguous ablation area as a result of the precise placement of the two laser catheters and effective coverage of the heterotopia (Fig. 6). The
patient tolerated the procedure well, but developed a complete right homonymous hemianopsia post-operatively that responded to administration of steroids to become an inferior temporal quadrantanopsia by 2 weeks and improved further by 6 weeks. Both patients were discharged home on post-operative day #1.
Seizure outcomes Patient 1 Following ablation the patient remained completely seizure free for one month. Her seizures then recurred, and by the time of her 3 months follow up the frequency was back to her baseline. With a change back to one of her prior medications (that had produced the best improvement but never total control prior to surgery), she again became seizure free (now at twelve months). Patient 2 Following ablation, the patient remained seizure free for 12 weeks. Seizures however recurred and were identical to those pre ablation. A repeat scalp video-EEG study showed interictal left temporal slowing and sharp waves, and left temporal onset seizures. Repeat MRI of the brain showed postoperative changes related to the ablation of the left PVNH. The patient underwent a craniotomy and intracranial
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Figure 6 (Patient 2): (A) T-2 coronal MRI prior to ablation, arrows show bilateral temporal—occipital PVNH. (B) Post ablation (3-month) T-2 coronal MRI, arrows show ablation along the two used trajectories.
electrode placement seven months post-ablation. Multiple strips and grids were placed to cover a wide cortical area over the frontal and temporal region, and a depth electrode was placed in the hippocampus. This evaluation demonstrated multiple interictal and ictal discharges arising chiefly from the mesial temporal lobe, as well as the temporal neocortex; there was no evidence of seizure activity from the area around the prior location of the PVNH. The patient underwent an anterior temporal lobectomy and amygdalohippocampectomy. He has remained seizure free for nine months following resection.
Discussion MR guided laser ablation has previously been employed in neurooncology, with good outcomes and acceptable safety profiles (Ascher et al., 1991; Kahn et al., 1994; Kettenbach et al., 1998). The Visualase system is the first MR guided laser ablation system approved by the FDA for soft tissue ablation in neurosurgery. Its safety has been demonstrated with the ablation of treatment resistant focal metastatic brain tumors and recurrent glioblastoma (Carpentier et al., 2012, 2011). More recently the use of this system for thermal destruction of epileptic foci in children (hypothalamic hamartoma, cortical dysplasia, tuberous sclerosis nodules) has shown promising results (Curry et al., 2012). Prior minimally invasive approaches for the management of PVNH have included stereotactic guided radiofrequency lesioning, (Schmitt et al., 2011) thermocoagulation (Catenoix et al., 2008; Guenot et al., 2004) and stereotactic radiosurgery (Sarkar et al., 2011). In this report, we present the first application of MRgLITT for the management of patients with PVNH associated epilepsy and demonstrate favorable outcomes in both patients. In the second patient, the results of the initial invasive video EEG
recordings revealed evidence of seizures originating from both the PVNH as well as the medial temporal structures. As previously seen in studies using intracranial EEG recordings from patients with PVNH, the seizure onset zone in these cases is rather broad, and better viewed as a network. Ablation of the presumed critical node (the PVNH) in this network may or may not ensure seizure control, (Aghakhani et al., 2005; Dubeau et al., 1995; Kothare et al., 1998) implying the existence of a widespread epileptogenic zone, (Kitaura et al., 2012; Li et al., 1997; Valton et al., 2008) and an existing ‘‘functional’’ relationship between the nodule and the overlying cortex (Tassi et al., 2005). The latter was the source of the second patient’s post ablation seizures that eventually prompted a standard temporal lobectomy with amygdalohippocampectomy. In this patient, due to the complex shape and large volume of the PVNH, we decided to use two separate ablation catheters to create the appropriately sized and shaped ablation zone. The advantage of using multiple probes for the ablation process enables the use of this technology for irregularly shaped, multiple, and complex lesions than might be accomplished otherwise. Additionally the implementation of the ablation process can be performed in a single or in staged procedures. We believe that in this patient the ablation of the PVNH was crucial for his seizure freedom since the predominance of seizure activity originated within PVNH tissue. In a phase II evaluation following MRgLITT no further seizures were recorded from depth electrodes placed in the small residual PVNH and seizures arose exclusively from the mesial temporal lobe and temporal neocortex. While we cannot know for certainty if a temporal lobectomy and amygdalohippocampectomy prior to the ablation of the PVNH would have rendered the patient seizure free, this is unlikely due to the patient’s ictal patterns in the first intracranial evaluation, that originated predominantly and clearly in the PVNH.
Stereotactic laser ablation Our view was that ablation of the PVNH using this minimally invasive approach would be worth trying prior to undergoing a more extensive resection, as it had atleast a modest chance of improving the clinical outcome in this patient with a epileptic network that involved structures crucial to memory and language. MRgLITT enabled us to target components of the epileptogenic network that are generally not amenable to microsurgical intervention. The PVNH tissue is located deep, and in both of these cases, was overlaid by eloquent cortex and by crucial white matter tracts. A traditional resective surgery would therefore have resulted in the disruption of normal uninvolved brain. The ability to monitor and enable closed loop control of the ablation in realtime maximizes the safety of this technique, as compared with other minimally invasive approaches. The incorporation of tractography data into planning and the ablation in the future might prevent inadvertent compromise of white matter fibers. Finally, the procedure is extremely well tolerated, with a very short period of hospitalization, and reduced costs. Moreover, its use does not preclude or make more challenging subsequent resections in cases of failure of seizure control or seizure recurrence. The experience presented in this study with MRgLITT in two patients with epilepsy secondary to PVNH is admittedly limited, in part to the rarity of patients suffering from epilepsy related to PVNH as well as the novelty of the technology. To the best of our knowledge, there are only 4 previously published cases in which PVNHs were tackled with minimally invasive approaches. Furthermore, it is unlikely that our results of relative seizure control in the absence of permanent neurological deficits could have been accomplished without the use of MRgLITT technology.
Conclusion MRgLITT possesses significant potential as a minimally invasive technique for ablation of PVNH, and more generally, as an adjunct in the surgical management of lesional epilepsy. In this study we demonstrate the safety, feasibility and limited efficacy of MRgLITT in PVNH-associated epilepsy, though its long-term efficacy will be revealed as more centers adopt the technology in the future.
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