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A historical perspective: Stereotactic lesions for the treatment of epilepsy James W. Leiphart a,b,c,d,*, Richard M. Young c, Donald C. Shields c a

Department of Neurosciences, Inova Medical System, Falls Church, VA, USA Department of Electrical and Computer Engineering, George Mason University, Fairfax, VA, USA c Department of Neurological Surgery, George Washington University Medical School, Washington, DC, USA d Department of Anatomy and Regenerative Biology, George Washington University, Washington, DC, USA b



Article history: Received 5 June 2013 Received in revised form 7 September 2013 Accepted 12 October 2013

Purpose: Most deep brain stimulation targets for movement disorders were derived from effective ablative surgery targets. Similarly effective lesion targets for epilepsy control may help refine brain stimulation targeting for epilepsy. A literature review of past stereotactic lesions for epilepsy treatment was performed to provide historical context and possible anatomical guidance for current and future attempts at controlling epilepsy with electrical stimulation. This work was undertaken to provide insights for electrical stimulation targets in epilepsy treatment based on outcomes from previous ablative therapies. Methods: A MEDLINE search was conducted for studies with the words ‘‘stereotactic surgery’’ and ‘‘epilepsy.’’ Post-operative results for 619 patients with stereotactic brain lesions targeting various anatomical foci were standardized using a modified Engel scale (1 ‘free of seizures’ to 3 ‘no significant improvement’). Each individual patient was entered into a database as a unique data point. Results: There was a statistically significant difference in reported seizure control among the different procedures and seizure types. The procedures that produced the best seizure control outcomes were the hippocampectomy, pallido-amygdalotomy, and amygdalohippocampectomy. Simple partial motor and combined generalized tonic clonic with complex partial seizure types demonstrated the best outcomes following surgery; complex partial and generalized tonic had the worst outcomes. Conclusions: The results of this study demonstrate the location of brain lesions has a significant effect on seizure control. Thus, future research designed to optimize brain stimulation targets for epilepsy control may be informed by previous ablative outcomes. ß 2013 British Epilepsy Association. Published by Elsevier Ltd. All rights reserved.

Keywords: Stereotactic Surgery Epilepsy surgery Literature review Lesionectomy Seizure

1. Introduction Epilepsy affects 4–8 out of 1000 people worldwide,1 and is characterized by recurrent seizures. Trauma is one of the two leading causes of epilepsy in the adult population younger than 65 years of age.2 Twenty to 30% of patients with epilepsy are not adequately controlled with medications,3 and only one-third of these patients are candidates for traditional surgical resections leaving a significant portion of this population with persistent seizures.4 Even among the paucity of patients in the United States with evaluations at Epilepsy Centers of Excellence,5 many are not candidates for surgical resection because: they present with a seizure focus that cannot be removed without causing significant disability, they have more than one focus of seizure activity, or they

do not have an identifiable seizure focus. Thus, strategies to electrically stimulate the brain are being developed as potential therapies to control intractable seizures.6–15 Stimulation strategies for the control of epilepsy vary widely, and multiple brain regions have been targeted with devices similar to those used for the treatment of movement disorders. Initial stimulation targets in patients with movement disorders were developed in light of prior experience with stereotactic lesions. In a similar way, clinical outcomes following stereotactic lesions in patients with epilepsy may help refine brain stimulation in the treatment of refractory epilepsy. To this end, we have performed a systematic review of stereotactic lesions for the treatment of epilepsy to evaluate the efficacy of each target lesion. 2. Methods

* Corresponding author at: Inova Department of Neurosciences, 3300 Gallows Road, Falls Church, VA 22042, USA. Tel.: +1 703 776 8310; fax: +1 703 776 4018. E-mail address: [email protected] (J.W. Leiphart).

A PubMed search was conducted using the words ‘‘epilepsy,’’ ‘‘surgery,’’ and ‘‘stereotactic.’’ Searches were limited to include only human subjects, and no date boundaries were set. Studies

1059-1311/$ – see front matter ß 2013 British Epilepsy Association. Published by Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.seizure.2013.10.006

Please cite this article in press as: Leiphart JW, et al. A historical perspective: Stereotactic lesions for the treatment of epilepsy. Seizure: Eur J Epilepsy (2013), http://dx.doi.org/10.1016/j.seizure.2013.10.006

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from the 2nd, 3rd, 4th and 5th World Congresses of Psychiatric Surgery were also included. This search returned 391 articles initially considered for this literature review, with dates ranging from 1965 to 2005. Strict inclusion criteria for the studies were used. To be included, each study must have employed focallytargeted stereotactic surgeries with one or two anatomical targets, patients must have undergone objective pre- and post-operative evaluations by a physician, and each study must have included lesions for the treatment of epilepsy. Moreover, only the longest patient follow-up data for each group of investigators was included, as some articles were written periodically on patients as they were followed for many years. Once these criteria had been met, our final dataset consisted of 619 patients treated with stereotactic lesions for epilepsy from 42 different studies. These 619 patients were then standardized according to a 3 point modified Engel scale based on post-operative physician evaluations. This scale ranged from 1 to 3, with 1 corresponding to a seizure free outcome, 2 indicating significant reduction in seizures, and 3 indicating minimal or no reduction in seizures. This scale was used as the dependent variable for analysis. Patients were divided into groups according to their ablative procedure. This resulted in 26 groups. Groups containing less than 5 patients were not analyzed due to their low statistical power. The remaining 16 procedure groups from 42 studies including 619 subjects with their distributions are shown in Table 1. A KruskalWallis test was performed to determine if there was a statistically significant difference in the outcomes from the 16 different anatomical targets using StatView1. Not all of the studies had clinical information that allowed for classification of seizure type. The studies with seizure classification data were also compared by seizure type using a Kruskal-Wallis test. This included 241 subjects from 21 studies.

Table 1 Number of patients analyzed by region of stereotactic lesion surgery for epilepsy.36–77 Area of lesion

Number of patients

Amygdalohippocampectomy Amygdalotomy Capsulotomy Cingulotomy Cortical Lesionectomy Dentatolysis Forelotomy Fornico-amygdalotomy Fornicotomy Fornicotomy with commisurotomy Hippocampectomy Hypothalotomy Pallido-amygdalotomy Pallidotomy Putaminectomy Thalamotomy

78 169 16 9 38 8 96 33 55 33 10 24 7 5 24 14

There was also a statistically significant difference in seizure control outcomes for different seizure types (p = 0.0018, Fig. 2). Patients with simple partial motor and those with combined generalized tonic–clonic with complex partial seizures demonstrated the best outcomes. Complex partial and generalized tonic types showed the worst outcomes. Table 2 shows the average seizure control outcome using the modified Engel scale for each lesion location by seizure type in patients with this data available. The low number of patients and missing data in several categories made meaningful statistical analysis impossible. 4. Discussion

3. Results The Kruskal-Wallis analysis determined that there was a statistically significant difference in seizure control outcomes among the different procedures shown in Fig. 1 (p = 0.026). The hippocampectomy (modified Engel scale: 1.4), pallido-amygdalotomy (1.71), and amygdalohippocampectomy (1.77) procedures resulted in the best seizure control outcomes. However, outcomes were poorest in patients undergoing cingulotomies (2.55), dentatolysis (2.36) and putamenectomies (2.13).

Brain stimulation techniques for the control of epilepsy7,16–20 include two basic approaches. In one approach a specific target, typically a nucleus or region of the cortex, is stimulated in an effort to reduce seizure frequency via effects through the entire brain.20 This method is advantageous since it can be utilized in patients who do not have a localized seizure focus. In the other approach, the identified seizure focus or foci are directly stimulated in an effort to disrupt seizures at their source.19 Although this requires an identified seizure focus, the advantage of this approach is that

Fig. 1. Average post-operative seizure control outcomes by target region for stereotactic lesion epilepsy surgeries. Modified Engel scale: (1) representing seizure freedom, (2) significant reduction in seizures, and (3) no significant reduction in seizures.

Please cite this article in press as: Leiphart JW, et al. A historical perspective: Stereotactic lesions for the treatment of epilepsy. Seizure: Eur J Epilepsy (2013), http://dx.doi.org/10.1016/j.seizure.2013.10.006

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Fig. 2. Average post-operative seizure control outcomes by seizure type for stereotactic lesion epilepsy surgeries. Modified Engel scale: (1) representing seizure freedom, (2) significant reduction in seizures, and (3) no significant reduction in seizures.

the stimulation can be performed in a responsive manner if electrophysiological evidence of seizure onset can be identified. Unlike the first approach, which requires continuous or pulsed stimulation, responsive stimulation has the potential to require less overall device output, and therefore a smaller battery source. Both methods have included stimulation parameters similar to those utilized in deep brain stimulation for movement disorders.8,14 Both methods have been utilized in an attempt to control seizures of various types originating from a variety of locations.19,20 Although the mechanisms by which deep brain stimulation modulates movement disorders are incompletely understood, many investigators believe that it acts by inhibiting or blocking the stimulated brain region, similar to the effects of stereotactic lesions.21,22 Non-seizure focus stimulation has been applied to various regions of the brain including the subthalamic nucleus,8,10 hippocampus,12,23,24 anterior thalamus,9,25 centromedian thalamus,11,25 cerebellum,26–28 and caudate.29 Attempts to stimulate the seizure focus/foci have also utilized several different targets, including the hippocampus and various cortical regions.6,7 In addition to findings from the above studies, historical lesion experience in seizure control may help guide the choice of stimulation targets. Stereotactic lesion surgery has the advantages of lower cost and elimination of the need for permanently implanted device which is at risk of infection, breakage, malfunction and would necessarily require a reoperation at some point for replacement of the electrical generator. The advantages of implanting a stimulator over producing a stereotactic lesion are the reversibility and adaptability of the therapy. Except for the subthalamic nucleus, lesion targets analyzed in the present study were similar to the various targets utilized in stimulation studies. These included lesions of the hippocampus,

thalamus, and cerebellum. In addition, many other regions were lesioned in the analyzed studies, suggesting the possibility of other potential targets. Not surprisingly, hippocampal lesions produced the best seizure reduction outcomes. This procedure is essentially a hippocampectomy utilizing a minimally invasive stereotactic approach. Open anterior temporal lobectomy with hippocampectomy has been extensively studied, and has demonstrated the best seizure control outcomes among all epilepsy surgery procedures.30–32 Moreover, hypothalotomy patients demonstrated good seizure control outcomes, as this procedure was performed exclusively for the treatment of hypothalamic hamartomas. Likewise, lesional epilepsy surgeries tended to have better outcomes than non-lesional surgeries. Of interest, the amygdala was not targeted for stimulation, although the amygdalotomy resulted in better seizure control outcomes when utilized in combination with lesions at other sites like the amygdalohippocampectomy, the fornico-amygdalotomy, and the pallodo-amygdalotomy. Nonetheless, amygdalotomy alone did not produce clinically significant seizure control outcomes. Thalamotomy and cortical lesionectomy procedures demonstrated favorable seizure control outcomes – providing further justification for their use as targets in the larger clinical studies of brain stimulation for epilepsy.6,7,16–18 Of note, one procedure that had surprisingly good seizure control outcomes was the forelotomy. The fields of Forel have not been stimulated for attempted seizure control, but this region may deserve consideration in future studies. The closest analogous procedure to cerebellum stimulation would be the dentatolysis, which had poor seizure control outcomes. Many of the studies reviewed had sufficient detail to draw conclusions concerning seizure control outcomes from stereotactic lesions. Patients showing the greatest reduction in seizures were those that had simple partial motor seizures. This was unexpected

Table 2 Table of average post-operative seizure control outcomes by seizure type and target region for stereotactic lesion epilepsy surgeries. Modified Engel scale: (1) representing seizure freedom, (2) significant reduction in seizures, and (3) no significant reduction in seizures. The number within the parentheses is the number of patients in each group. CP: complex partial; GT: generalized tonic; GTC: generalized tonic clonic; SP: simple partial. CP


Amygdalohippocampectomy Amygdalotomy Capsulotomy Cortical lesionectomy Dentatolysis Forelotomy Fornico-amygdalotomy Fornicotomy Hypothalotomy

1.7 2.1 – – – 3.0 2.1 2.2 –

(23) (18)

(11) (7) (12)





SP Psychic

– – 1.5 (4) – – 2.2 (11) – – –

– 1.5 2.2 – 2.0 1.4 – 1.9 –

– 1.0 (2) – 1.0 (2) – 2.3 (3) – –

– – – 1.0 (4) 2.7 (3) 1.3 (20) – – –

– 1.0 (1) – – – – – – 1.8 (12)

(13) (11) (4) (32) (42)

Please cite this article in press as: Leiphart JW, et al. A historical perspective: Stereotactic lesions for the treatment of epilepsy. Seizure: Eur J Epilepsy (2013), http://dx.doi.org/10.1016/j.seizure.2013.10.006

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for two reasons. First, in previous epilepsy surgery series, simple partial seizures did not have the best post-operative outcomes.33 Second, the stereotactic lesion surgeries that demonstrated the best outcomes were those that had hippocampectomies. Complex partial seizures are associated with hippocampal onset, so complex partial seizures would be expected to have the best outcomes.34 This may be due to inconsistent reporting of seizure types among the various studies. Only 39% of the patients with reported outcome data had reliable information to determine seizure type. Combined generalized tonic clonic and complex partial seizures had the next best outcomes. These cases probably represented complex partial seizures with secondary generalization. These good outcomes agree with epilepsy surgery studies that showed the best outcomes with complex partial seizures.35 Complex partial seizures alone had the worst post-operative outcomes from stereotactic lesion surgeries. Again, this surprising result calls into question the determination of seizure type in these studies. 5. Conclusions This study was designed to review potentially useful historical data concerning seizure control outcomes from stereotactic brain lesions. Lesions involving the hippocampus, amygdala, thalamus, and cortical foci showed the best seizure reduction outcomes. This corresponds with targets currently used in brain stimulation for epilepsy control. Seizure types that responded best to stereotactic lesioning were simple partial seizures and combined generalized tonic clonic/complex partial seizures. These findings may help optimize the selection of targets and patients appropriate for stimulation epilepsy surgery.











Conflicts of interest statement 21.

We wish to confirm that there are no known conflicts of interest associated with this publication and there has been no significant financial support for this work that could have influenced its outcome.



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G Model

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Please cite this article in press as: Leiphart JW, et al. A historical perspective: Stereotactic lesions for the treatment of epilepsy. Seizure: Eur J Epilepsy (2013), http://dx.doi.org/10.1016/j.seizure.2013.10.006

A historical perspective: stereotactic lesions for the treatment of epilepsy.

Most deep brain stimulation targets for movement disorders were derived from effective ablative surgery targets. Similarly effective lesion targets fo...
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