Prognostic value of intracranial seizure onset patterns for surgical outcome of the treatment of epilepsy
Introduction
Resective surgery can achieve seizure freedom in 40% to 70% of patients with drug-resistant epilepsy (Wiebe et al., 2001, de Tisi et al., 2011, Kumar et al., 2013). Successful outcome of surgery depends on accurate identification of the epileptogenic zone (Engel et al., 1993, Luders et al., 2006, Jette and Wiebe, 2013). At present, a variety of non-invasive techniques are initially used to identify the epileptogenic zone, including interictal and ictal scalp electroencephalography (Adachi et al., 1998, Alarcon et al., 2001, Alarcon et al., 2012b), neuroimaging (Koutroumanidis et al., 2004, Duncan, 2010) and neuropsychology (Akanuma et al., 2003). However, in approximately 25% of patients assessed for surgery, non-invasive techniques are non-localising or non-concordant, and assessment with intracranial electrodes may be necessary to identify the epileptogenic zone (Alarcon et al., 2006).
The EEG recorded with intracranial electrodes shows larger amplitude and less muscle artefacts than the scalp EEG. In addition, intracranial recordings show a wider variety of interictal and ictal abnormalities than the scalp EEG (Fernandez Torre et al., 1999b, Kissani et al., 2001) not necessarily restricted to the ictal onset zone (Alarcon et al., 1995, Fernandez Torre et al., 1999a, Kissani et al., 2001). Interictal slowing of the background activity occur at or around the area of seizure onset in around 80% of patients assessed with chronic intracranial recordings (Valentin et al., 2014). In 40–100% of patients, spontaneous interictal epileptiform discharges occur independently at the seizure onset zone and elsewhere, including contralateral cortex (Alarcon et al., 1994, Fernandez Torre et al., 1999b).
Despite the presence of interictal abnormalities, the interpretation of chronic intracranial recordings still heavily relies on the identification of the ictal onset zone, i.e., the area where seizures start on intracranial recordings. A difficulty arises from the fact that the onset of focal seizures can be associated with a variety of EEG patterns, which are not necessarily focal in distribution (Alarcon et al., 1995). Approximately two thirds of focal seizures start with a run of focal fast activity, sharp waves, spikes or slow waves lasting for a few seconds (Alarcon et al., 1995). However, in one third of seizures, focal changes are preceded by more widespread patterns, such as a diffuse attenuation of the background activity (diffuse electrodecremental event or DEE) (Alarcon et al., 1995). In many human recordings, these sustained ictal changes are immediately preceded by a single epileptiform discharge (preceding epileptiform discharge, or PED), which can show a widespread or bilateral distribution and is associated with a prominent slow wave. A similar phenomenon described as “leading spike” has been reported in 15 children with epileptic spasms (Asano et al., 2005). Although PEDs are transitory phenomena resembling interictal activity, their association with seizures is obvious, as they consistently occur immediately preceding the onset of the more sustained ictal patterns described above. The physiological and clinical significance of such widespread changes at seizure onset in focal epilepsy are unclear.
To simplify wording throughout the paper, the ictal onset patterns which typically last for several seconds (DEE and runs of focal fast activity, sharp waves, spikes or slow waves) will be generically designated as “sustained ictal onset patterns” (SIOP). PEDs can precede any type of SIOP and consequently will be analysed separately. The term “seizure onset patterns” will include SIOPs and PEDs.
To the best of our knowledge, the prognostic significance of PEDs has not been reported in focal epilepsies. Its removal is associated with favourable outcome in infantile spasms (Asano et al., 2005). Several authors have studied the value of intracranial SIOPs to predict surgical outcome (Lieb et al., 1986, Spencer et al., 1992, Alarcon et al., 1995, Jung et al., 1999, Kutsy et al., 1999, Lee et al., 2000, Zaatreh et al., 2003, Wetjen et al., 2009, Holtkamp et al., 2012, Dolezalova et al., 2013). These studies suggest that the presence of focal fast activity at seizure onset appears to be associated with seizure relief after resective surgery. However, the prognostic value of the more widespread SIOPs is unclear. DEE is one of the most common SIOP, occurring in as many as 60% of patients assessed with intracranial electrodes (Alarcon et al., 1995, Zaatreh et al., 2003, Perucca et al., 2013) and is the first SIOP in about a third of seizures recorded with intracranial electrodes (Alarcon et al., 1995). Early studies on a very limited number of cases suggested that the presence of DEE does not significantly affect surgical outcome (Alarcon et al., 1995). Unfortunately, larger studies on the prognostic value of ictal onset patterns have not usually included DEE in their analysis (Spencer et al., 1992, Lee et al., 2000, Wetjen et al., 2009, Holtkamp et al., 2012, Park et al., 2012). One publication suggested that the presence of DEE may be associated with poor surgical outcome in temporal lobe epilepsy (Dolezalova et al., 2013), and one abstract has reported that the same may occur in extratemporal epilepsy (Zaatreh et al., 2003).
In the present work, we study the prognostic value with regard to seizure control and pathology of the following intracranial seizure onset patterns: PED, DEE, runs of focal fast activity (FA), spikes, sharp waves, alpha or slow activity. We report a series of 69 consecutive patients undergoing resective surgery for the treatment of epilepsy, the largest study published to date, including temporal and extratemporal patients. We also analyse the prognostic significance of widespread and bilateral PEDs. Preliminary results have been published in abstract form (Jimenez-Jimenez et al., 2013).
Section snippets
Patients
The study initially included all 74 patients who underwent cortical resective surgery for the treatment of epilepsy after assessment with intracranial electrodes implanted at King’s College Hospital between 08th of November 1999 and the 23th of December 2010 and had postsurgical follow-up of 12 months or longer. The following patients were excluded: (a) Patients who had no seizures during telemetry (1 patient), (b) Patients who underwent hemispherectomy for the treatment of Rasmussen Disease (1
Patients
Among all 69 patients, 31 (45%) patients were female and 38 (55%) were male. The mean age at onset of epilepsy was 10.73 years (SD = 9.07). The average age at resection was 31.8 years (SD = 13.0). The mean follow-up period was 42.15 months (SD = 30.1). Table 1 summarises patients’ details. Fifty-one patients (73.9%) underwent temporal lobe resections, 13 (18.8%) had frontal resections, two (2.9%) patients underwent parietal resections, two (2.9%) had occipital resections, and one patient underwent an
Discussion
The purpose of this study is to estimate the prognostic value of the seizure onset pattern to predict seizure control and pathology after epilepsy surgery. We found that FA was associated with favourable surgical outcome, whereas DEE was associated with poor surgical outcome. The presence or topographic extension of PEDs was not correlated with outcome. There is no clear association between pathology and seizure onset pattern.
Conclusion
In the present paper, we characterise the incidence and prognostic value of focal, widespread and bilateral PEDs. FA, FA-DEE, DEE and PED are the most common SIOPs. The presence of FA as SIOP was associated with favourable surgical outcome, whereas DEE was associated with poor surgical outcome. Presence or topographic extension of PEDs was not correlated with good or poor outcome. There is no clear association between pathology and seizure onset patterns.
Disclosure
None of the authors has any sources of support regarding this study, or any conflict of interest to disclose.
Funding
The National Secretariat for Higher Education, Science, Technology and Innovation of Ecuador (SENESCYT) funded this work as part of a PhD degree.
References (49)
- et al.
The effects of electrical stimulation of A and C visceral afferent fibres on the excitability of viscerosomatic neurons in the thoracic spinal cord of the cat
Brain Res
(1990) - et al.
Power spectrum and intracranial EEG patterns at seizure onset in partial epilepsy
Electroencephalogr Clin Neurophysiol
(1995) - et al.
In vivo neuronal firing patterns during human epileptiform discharges replicated by electrical stimulation
Clin Neurophysiol
(2012) - et al.
Value of scalp delayed rhythmic ictal transformation (DRIT) in presurgical assessment of temporal lobe epilepsy
Clin Neurophysiol
(2012) - et al.
High frequency oscillations in the intact brain
Prog Neurobiol
(2012) - et al.
The long-term outcome of adult epilepsy surgery, patterns of seizure remission, and relapse: a cohort study
Lancet
(2011) - et al.
Intracranial EEG seizure onset patterns in unilateral temporal lobe epilepsy and their relationship to other variables
Clin Neurophysiol
(2013) - et al.
Comparison of sphenoidal, foramen ovale and anterior temporal placements for detecting interictal epileptiform discharges in presurgical assessment for temporal lobe epilepsy
Clin Neurophysiol
(1999) - et al.
Sensitivity of recordings at sphenoidal electrode site for detecting seizure onset: evidence from scalp, superficial and deep foramen ovale recordings
Clin Neurophysiol
(2001) - et al.
Preoperative estimation of seizure control after resective surgery for the treatment of epilepsy
Seizure
(2013)
The pathophysiologic relationships between lesion pathology, intracranial ictal EEG onsets, and hippocampal neuron losses in temporal lobe epilepsy
Epilepsy Res
Ictal high-gamma oscillation (60–99 Hz) in intracranial electroencephalography and postoperative seizure outcome in neocortical epilepsy
Clin Neurophysiol
Interictal estimation of intracranial seizure onset in temporal lobe epilepsy
Clin Neurophysiol
Predictive value of interictal epileptiform discharges during non-REM sleep on scalp EEG recordings for the lateralization of epileptogenesis
Epilepsia
Lateralising value of neuropsychological protocols for presurgical assessment of temporal lobe epilepsy
Epilepsia
Surgical techniques
Preoperative assessment
Intracerebral propagation of interictal activity in partial epilepsy: implications for source localisation
J Neurol Neurosurg Psychiatry
Origin and propagation of interictal discharges in the acute electrocorticogram. Implications for pathophysiology and surgical treatment of temporal lobe epilepsy
Brain
Lateralizing and localizing values of ictal onset recorded on the scalp: evidence from simultaneous recordings with intracranial foramen ovale electrodes
Epilepsia
Is it worth pursuing surgery for epilepsy in patients with normal neuroimaging?
J Neurol Neurosurg Psychiatry
Origin and propagation of epileptic spasms delineated on electrocorticography
Epilepsia
Imaging in the surgical treatment of epilepsy
Nat Rev Neurol
Surgical treatment of the epilepsies
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Drs. A. Valentín and G. Alarcón are joint senior authors.