From SEEG Explorations to Surgical Interventions

Introduction

The fundamental objective of SEEG is to facilitate the strategic planning and execution of surgical intervention(s) aimed at cessation of epileptic activity, translated into seizure freedom or at least seizure reduction for the patient. Potentially curative surgery includes the resection, disconnection, or ablation of cortical regions producing epileptogenic activity while ensuring the preservation of essential brain function. The decision to undertake either resection or ablation depends upon a comprehensive analysis of SEEG findings, necessitating the collective input of a multidisciplinary cohort comprising neurologists, neurosurgeons, neuroradiologists, and neuropsychologists, united in the pursuit of optimizing patient outcomes.

This chapter will discuss the transition from the interpretive phase of SEEG to the ensuing surgical interventions, which will include resection, ablative procedures, and neuromodulation interventions when curative options are not available.

General aspects of SEEG explorations relevant to the final surgical interventions

The foundational precepts governing stereo-electroencephalography (SEEG) investigations play an indispensable role in translating diagnostic insights into efficacious surgical outcomes. ^, ^, This segment details six key facets of SEEG explorations that directly impact ultimate surgical interventions. Regardless of the nature of the surgical modality employed, these six tenets form the basis of subsequent decisions and procedural maneuvers. These principles are:

1.

Deliberate Patient Selection and Scrutiny: The inaugural principle of SEEG exploration underscores the imperative of meticulous patient selection and evaluation in contemplation of surgical intervention. This process assumes paramount importance as it precludes the engagement of SEEG methodologies in individuals unsuitable for surgical candidacy from inception. The selection criteria (requiring sufficient team expertise to determine this important step) hinge upon a comprehensive clinical assessment encompassing seizure semiology, neuroimaging correlates, and responsiveness to antiepileptic pharmacotherapy. Patients demonstrating unfavorable prognostic indicators for localizable epileptogenic zones (EZs) or evincing reluctance toward curative surgical intervention are deemed unsuitable candidates for SEEG. ^,
2.

Rigorous Implantation Strategizing: The second principle of SEEG exploration revolves around the strategy of SEEG electrode implantation. In the context of resective inquiries, this strategizing necessitates delineation of the EZ localization, anatomical extent, and boundary demarcations. Parameters such as electrode placement, quantity, and orientation must duly encapsulate the suspected EZ, allied functional domains, and the anatomical continuum of prospective treatable regions to inform subsequent surgical interventions. ^,

The SEEG exploratory process provides multiple converging opportunities to delineate and confirm the EZ. The approach is based on sampling sets of connected brain structures (networks) rather than attempting to achieve “coverage”. Direct electrical stimulation is an essential step in evaluating the EZ.
3.

Functional Elucidation: SEEG allows interrogation of functional cerebral substrates, inclusive of eloquent cortical territories and white matter tracts, with the aim of mitigating the postoperative risk of neurological compromise. Functional exploration mandates the identification of structures necessitating preservation during forthcoming surgical endeavors. ^,^,
4.

Anatomical and Functional Constraints: Knowledge of anatomical and functional constraints assumes primacy in shaping the contours of final surgical intervention. This entails the delineation of safe surgical trajectories, circumvention of eloquent cortical territories, and the surgical strategy of complete EZ resection or ablation while safeguarding essential neurological functionalities.
5.

Multidisciplinary Synergy: SEEG inquiries and subsequent surgical undertakings necessitate good communication and teamwork among neurologists, neurosurgeons, neuroradiologists, neuropsychologists, and allied specialists. Multifaceted deliberations engender a comprehensive evaluative milieu conducive to optimized surgical planning.
6.

Ethical Deliberations: Ethical considerations, foregrounding patient autonomy, beneficence, and nonmaleficence, are paramount in the context of SEEG investigations and ensuing surgical modalities. Prerequisites such as informed consent, deference to patient preferences, and circumspect evaluation of potential risks vis-à-vis benefits, emerge as axiomatic imperatives.

In summation, the foundational tenets underpinning SEEG explorations also guide final surgical interventions for epilepsy patients. The combination of careful patient selection, implantation planning, functional elucidation, anatomical and functional constraints, multidisciplinary collaboration, and ethical probity collectively help determine surgical outcomes after SEEG-guided interventions.

Different types of SEEG-guided interventions

Several surgical techniques may be deployed for cortical and subcortical interventions subsequent to SEEG evaluation:

1.

Asleep Resections/Disconnections: This approach entails the excision (or disconnection) of epileptogenic tissue utilizing conventional microsurgical methodologies with patients under general anesthesia. The surgical execution adheres rigorously to the predefined plan, ensuring comprehensive removal/disconnection of the targeted tissue while safeguarding vital surrounding brain tissue and arteries and veins. Notably, functional assessment is largely completed during the SEEG evaluation, obviating the need for supplementary functional information to ensure the safety of the resection. However, asleep sensorimotor mapping can be used in anatomically relevant surgeries under general anesthesia as needed.
2.

Awake Resections: In instances where the resection implicates eloquent cortical territories, an awake craniotomy may be warranted. This modality enables real-time mapping of functional cerebral areas, thereby ensuring the preservation of eloquent cortex during the resection, while complementing the functional insights garnered during the extra-operative SEEG evaluation.
3.

Minimally Invasive Techniques: In select clinical scenarios, minimally invasive modalities such as laser interstitial thermal therapy (LITT) or radiofrequency thermocoagulation (RFTC) may be employed to ablate epileptogenic foci. These techniques confer the advantage of minimal collateral damage to surrounding brain parenchyma coupled with expedited patient recovery. ^,^,^,^,
4.

SEEG-Guided Neuromodulation: When curative resections are precluded either due to inadequate localization or the inherent risk of neurological sequelae, neuro-modulatory interventions emerge as a palliative recourse. In certain contexts, SEEG data may inform the deployment of neuromodulation modalities such as deep brain stimulation (DBS) or responsive neurostimulation (RNS) although how best to choose DBS target and protocol at the individual patient level remains an area of active clinical research. In bilateral mesial temporal epilepsy, bilateral amygdalo-hippocampal depth electrode placement tethered to either an open-loop (DBS) or closed-loop (RNS) configuration may be contemplated. RNS is the preferred modality in the United States, as DBS of bilateral hippocampi is not FDA approved; while hippocampal DBS is preferred in many other parts of the world, where RNS is not yet an option. Of course, we recognize that some world regions do not have any access to intracranial DBS after SEEG. In cases where the EZ spans beyond the mesial temporal compartment, involving adjacent neocortical territories bilaterally, the indications and outcomes of SEEG-guided neuromodulation are less well known and more research is needed.

Determinant factors related to SEEG-guided intervention strategies selection

SEEG-guided interventions are adapted to individual patients, contingent upon the comprehensive outcomes and interpretations derived from that patient’s evaluation. Enumerated below are delineations concerning the determinants governing the judicious selection of SEEG-guided procedures:

1.

Location and Volume of the Epileptogenic Zone (EZ): In neocortical epilepsies, the treatment modality post-SEEG evaluation is markedly influenced by the dimensions and morphological complexities of the EZ. Robustly sized EZs (>2 cm ) or those evincing intricate contours typically necessitate direct resection or disconnection, affording superior outcomes vis-à-vis minimally invasive modalities such as laser interstitial thermal therapy (LITT). Microsurgical interventions proffer heightened precision in anatomical resections, particularly advantageous for extensive EZs, which may pose geometrical challenges for laser-based therapies. Conversely, in instances where the EZ is restricted to deep-seated cortical locations with smaller volume, SEEG-guided LITT is a minimally invasive promising alternative to open surgery. ^,^,

In neocortical epilepsy, LITT may be particularly beneficial for patients harboring deep-seated, focal, and compact EZs, such as the insular-opercular, mid to posterior cingulate, and mesial temporal regions. In the insula, particularly the posterior superior part, open surgical resection carries the risk of stroke of one of the small deep perforating arteries off the middle cerebral artery M3 branches located within the insular sulci. A very small infarction in the corona radiata in this region can result in a clinically significant patient deficit. Use of LITT to ablate insular opercular epilepsy is gaining traction in the epilepsy community. Existing data underscore notable rates of seizure freedom, ranging from 53% to 69%, following resection or ablative interventions targeting insulo-opercular regions, predominantly observed in cases accompanied by associated lesions. However, specific data pertaining to seizure outcomes in nonlesional insulo-opercular epilepsy remain scant. Nonlesional pure insular epilepsies are less common. Most of these patients have a combined insulo-opercular EZ revealed by SEEG that then must be subsequently treated by resection or ablation.

If SEEG identifies the EZ as restricted to the motor or posterior cingulate, many epilepsy centers are now using LITT. The motor cingulate requires surgical resection along the medial bank of the hemisphere, below the leg Rolandic cortex, while the posterior cingulate can be quite deep within the medial brain, below the precuneus. These areas are surgically accessible but pose some increased risk due to their specific locations and associated venous anatomy abutting the sagittal sinus. LITT is being used more as a tool to carry out corpus callosotomy, and similar strategies are being applied to the cingulate region, just above the corpus callosum.

In scenarios where the EZ is confined to mesial temporal structures, microsurgical selective amygdalohippocampectomy is the time-tested surgical strategy, but LITT also warrants consideration. Whether to use open surgical resection, LITT, or brain stimulation to treat a mesial temporal EZ depends on several factors including cerebral dominance, MRI findings (mesial temporal sclerosis, low grade epilepsy associated tumor, MRI normal), patient neuropsychological function/risk of worsening, and surgeon experience.
2.

Proximity to Eloquent Cortex: The adjacency between the EZ and functionally vital areas delineated by SEEG constitutes a key determinant in the selection of surgical interventions post-SEEG assessment. Instances of close spatial juxtaposition often necessitate surgical resection guided by intraoperative functional mapping, with awake procedures frequently warranted for enhanced assessment of language-associated cortical and subcortical domains. Furthermore, intraoperative neuromonitoring techniques, encompassing somatosensory evoked potentials, motor evoked responses, and direct cortical and subcortical stimulation, can help in evaluating sensory and motor function integrity. Awake patient testing during SEEG-guided LITT procedures is challenging and rarely attempted, as the patient needs to hold perfectly still within the MRI scanner during the procedure. In clinical scenarios where there is considerable overlap between the EZ and functionally important territories, invasive monitoring modalities such as responsive neurostimulation (RNS) or deep brain stimulation (DBS), should be considered as palliative interventions.
3.

Patient Expectations: The consideration of patient expectations and aspirations assumes paramount significance in delineating the post-SEEG surgical treatment modality. While the attainment of sustained seizure freedom remains the primary objective, proximity between the EZ and functional territories may result in unacceptable risk of neurological compromise with surgical resection or ablation. In such scenarios, patients may opt for palliative modalities such as RNS or DBS (if available) to assuage seizure burden while minimizing the prospect of significant functional deficits. A comprehensive elucidation of risks and benefits is imperative in tailoring the treatment paradigm in consonance with the individualized needs and risk tolerance of the patient.

The Talairach space and the translation to the three-dimensional surgical anatomy

The conceptual framework of Talairach space, delineated by coordinates derived from the anterior and posterior commissures along with the midsagittal plane, has revolutionized neurosurgical precision by facilitating the precise targeting of discrete cerebral regions for therapeutic interventions. This pivotal innovation has not only heralded a paradigm shift in neurosurgical planning and execution but also constitutes a fundamental cornerstone in translating SEEG interpretations into actionable surgical strategies ( Fig. 12.1 ). To ensure a seamless transition, consideration of three critical aspects is imperative:

1.

Effective Communication Between Epileptologist and Neurosurgeon: Central to this translational process is the cross-disciplinary exchange between epileptologists and neurosurgeons, both preoperatively and intraoperatively. This collaborative dialog necessitates a comprehensive discourse encompassing the localization and volumetrics of resection, potential overlaps with functional cortical and subcortical territories, and a holistic understanding of patient expectations. The synthesis of complementary expertise spanning clinical semiology, electrophysiology, and structural and functional neuroanatomy is indispensable in formulating a precise tailored resection plan that optimizes both efficacy and safety.
2.

Cognizance of Anatomical and Functional Variables: A nuanced understanding of anatomical and functional variables that may impede the comprehensive resection of the epileptogenic zone or necessitate procedural modifications is imperative. For instance, careful attention to vascular structures during temporal lobe resections is paramount to avoid inadvertent compromise of critical structures.
3.

Intraoperative Recognition of Electrode Positions: Accurate localization of electrode positions relative to cortical anatomy is fundamental in ensuring the efficacy and safety of SEEG-guided procedures. Using advanced imaging modalities and computer-assisted software, neurosurgeons can construct detailed patient-specific anatomical models, enabling precise intraoperative navigation. Failure to rigorously plan electrode positions during the intraoperative phase may compromise the precision of prior localization efforts, leading to unpredictable neurological deficits and procedural failures. Following the completion and interpretation of SEEG-guided procedures, the electrodes are typically removed, necessitating a reliable method for precisely localizing the explored cortical and subcortical areas. Various intraoperative techniques for recognizing SEEG-recorded cortical regions exist, contingent upon the availability of specific imaging technologies, surgeon preferences, and the surgical site ( Fig. 12.2 ). These methods, whether employed individually or in combination, serve to enhance localization accuracy. Here, we delineate several such approaches:
- A.
  
  Recognition of Superficial Cortical and Vascular Anatomy: Via fusion of pre-operative MRIs with SEEG post-operative CTs, surgeons can discern cortical regions and associated sulci patterns, facilitating intraoperative identification. This analysis enables visualization of the SEEG-recorded areas within the context of unique anatomical configurations. Additionally, recognition of cortical veins, particularly major branches, provides further localization cues, while arteries, though more subtle, may also serve as fiducial markers.
- B.
  
  Recognition of SEEG Electrode Entry-Point Sites: Among the most precise methods of intraoperative electrode localization is the recognition of electrode entry points in conjunction with superficial cortical and vascular anatomy. Electrode scars, unaffected by brain shifts during surgical manipulations, serve as precise markers of prior electrode positions. Through careful intraoperative comparison with cortical landmarks, these scars facilitate the identification of explored cortical areas and regions slated for treatment. This method extends beyond superficial cortical regions to encompass deep cortical territories, contingent upon electrode orientation and patient positioning.
- C.
  
  Application of Intraoperative Neuronavigational Devices: Neuronavigation, integrated with visualization techniques such as cortical anatomy and residual electrode markers, provides a robust method for intraoperative localization. By digitally fusing post-SEEG implanted CT images with pre-resection structural MRIs, surgeons can readily identify prior electrode placements. However, reliance solely on neuronavigation may be limited by tissue displacement during craniotomy and errors in registration, necessitating caution to mitigate potential complications.
- D.
  
  Intraoperative Confirmation of Extraoperative Functional Mapping: Intraoperative confirmation of extraoperative functional mapping through direct electrical stimulation offers precise validation of cortical localization and treatable areas. Despite its precision, this method is susceptible to variations in anesthesia levels, body temperature, and probe positioning. Moreover, its efficacy hinges on the combined expertise of clinical neurophysiologists and the operating surgical team and necessitates integration with complementary nonelectrophysiological methods to optimize outcomes.
FIG. 12.2

Method of intraoperative recognition of SEEG electrodes. The figure describes the method used by the authors to recognize the anatomical position of previous SEEG electrodes in order to guide SEEG resections. Panel A depicts the SEEG implantation schema of an exploration in the dominant temporo-occipital areas. Here, the SEEG evaluation reviewed the location of a restricted EZ located at the basal surface of the temporo-occipital areas, at the vicinity of electrode F′ and O′. Panel B illustrate the position of electrode F′, with the anatomical localization of the EZ in the fusiform gyrus. Panel C illustrate the skin incision planning as well as the areas of resection based on the superficial scar markers left by the SEEG electrode orthogonal implantations. Panel D depicts the exposure of the temporo-occipital bone structures. Note the presence of the pinholes from the previous SEEG electrode implantation, demarcating the subsequent craniotomy. Panel E and F illustrate the exposure of the dura and the adjacent cortical areas related to the electrodes of interest.