Outcome of intracranial electroencephalography monitoring and surgery in magnetic resonance imaging-negative temporal lobe epilepsy
Introduction
The role of surgical resection has been well established in medically intractable temporal lobe epilepsy (TLE) (Wiebe et al., 2001, Yoon et al., 2003, Cohen-Gadol et al., 2006, Schmidt and Stavem, 2009). Seizure-free outcome rates after resective surgery average around 70–80% in patients with hippocampal atrophy and concordant interictal and ictal electroencephalographic (EEG) discharges (Berkovic et al., 1995, Cascino, 2004). Unfortunately, the success rate is much lower in patients with non-lesional TLE (Berkovic et al., 1995, Holmes et al., 2000, Chapman et al., 2005, Tatum et al., 2008, Bell et al., 2009). Given the fact that mesial temporal structures are important for memory, physicians may be more reluctant to recommend anterior temporal lobectomy, which includes the mesial temporal structures, when no structural abnormality is identified on magnetic resonance imaging (MRI). In these complicated patients, intracranial EEG (iEEG) monitoring is often required to guide temporal lobe resection.
Because increased complication rates are related to longer monitoring and a greater number of electrodes being implanted, the extent of electrode implantation for iEEG should be determined judiciously and should be limited to reduce the risk of complications (Hamer et al., 2002). The prognostic value of interictal spiking in intraoperative electrocorticography (ECoG) remains controversial. Luther et al. (2011) reported that intraoperative ECoG can be useful in a subset of patients with TLE and non-lesional MRI. However, other authors could not find correlation between seizure-free outcomes and complete resection of irritative zone on ECoG (Schwartz et al., 1997, San-juan et al., 2011, Wray et al., 2012). Therefore, the role of chronic extraoperative iEEG monitoring in patients with MRI-negative TLE remains important and deserves further study. The purpose of this study was to determine the yield of extraoperative iEEG monitoring in patients with MRI-negative TLE. In addition, we sought to determine the outcome of subsequent resective surgery in these patients.
Section snippets
Patient population
This study was approved by the Mayo Clinic Institutional Review Board. Patients were identified from the epilepsy surgery databases at Mayo Clinic, Jacksonville, Florida (January 1, 2005–December 31, 2012), Mayo Clinic, Rochester, Minnesota (January 1, 2000–December 31, 2012), and Mayo Clinic, Scottsdale, Arizona (January 1, 2000–December 31, 2012).
Noninvasive presurgical evaluations
Charts were reviewed to determine patient characteristics, including age at surgery, duration of epilepsy, seizure risk factors, history of status
Demographic characteristics
A total of 32 patients (3 patients from Arizona, 5 from Florida, and 24 from Minnesota) fit our inclusion criteria. Characteristics of these patients are summarized in Table 1. More than half of the cohort had at least 1 seizure risk factor. Three patients had a history of status epilepticus. The median age at surgery was 32 years (IQR, 23–40 years). Our patients had a long history of seizures, averaging 9.5 years (IQR, 4.5–18 years). They also had a high seizure burden, with a median seizure
Discussion
Studies have shown that epilepsy surgery can be effective in patients with MRI-negative TLE. However, the reported success rate of 40–60% is much lower than that for patients with MRI-apparent structural abnormality concordant with the seizure onset zone (Berkovic et al., 1995, Cohen-Gadol et al., 2006, Bell et al., 2009, Vale et al., 2012). In addition, language and memory function are often supported by regions found in close proximity to the epileptogenic zone, making physicians more
Conclusion
In summary, our study has demonstrated the informative role that iEEG evaluations can play in patients with TLE and negative MRI. Anterior temporal lobectomy guided by iEEG in these patients is associated with a high rate of freedom from postsurgical seizures, which is comparable to that in patients with MRI-detected temporal lobe lesions. It is also important to identify neocortical temporal lobe seizure focus in patients with MRI-negative TLE, because surgery that is restricted to the focus
Conflict of interest
None.
Funding source
None.
Acknowledgments
We confirm that we have read the Journal's position on issues involved in ethical publication and affirm that this report is consistent with those guidelines.
References (44)
Surgical treatment for epilepsy
Epilepsy Res.
(2004)- et al.
Outcome after surgery in patients with refractory temporal lobe epilepsy and normal MRI
Seizure
(2000) - et al.
Pre-surgical evaluation and surgical outcome of 41 patients with non-lesional neocortical epilepsy
Seizure
(2002) - et al.
The prognostic role of electrocorticography in tailored temporal lobe surgery
Seizure
(2011) - et al.
Ictal EEG remains the prominent predictor of seizure-free outcome after temporal lobectomy in epileptic patients with normal brain MRI
Seizure
(2008) - et al.
Efficacy of temporal lobe surgery for epilepsy in patients with negative MRI for mesial temporal lobe sclerosis
J. Clin. Neurosci.
(2012) - et al.
Ictal clinical and scalp-EEG findings differentiating temporal lobe epilepsies from temporal ‘plus’ epilepsies
Brain
(2007) - et al.
Epilepsy surgery outcomes in temporal lobe epilepsy with a normal MRI
Epilepsia
(2009) - et al.
Neocortical temporal lobe epilepsy
Epilepsy Res. Treat.
(2012) - et al.
Preoperative MRI predicts outcome of temporal lobectomy: an actuarial analysis
Neurology
(1995)
Hippocampal sclerosis following brief generalized seizures in adulthood
Neurology
Seizure outcome after epilepsy surgery in patients with normal preoperative MRI
J. Neurol. Neurosurg. Psychiatry
Long-term outcome of epilepsy surgery among 399 patients with nonlesional seizure foci including mesial temporal lobe sclerosis
J. Neurosurg.
Association of ipsilateral motor automatisms and contralateral dystonic posturing: a clinical feature differentiating medial from neocortical temporal lobe epilepsy
Arch. Neurol.
Localization of temporal lobe foci by ictal EEG patterns
Epilepsia
Outcome with respect to epileptic seizures
Characteristics of medial temporal lobe epilepsy: I. Results of history and physical examination
Ann. Neurol.
Ictal semiology in hippocampal versus extrahippocampal temporal lobe epilepsy
Brain
The role of the limbic system in experiential phenomena of temporal lobe epilepsy
Ann. Neurol.
Complications of invasive video-EEG monitoring with subdural grid electrodes
Neurology
Long-term epilepsy surgery outcomes in patients with MRI-negative temporal lobe epilepsy
Epilepsia
Neocortical temporal lobe epilepsy
J. Clin. Neurophysiol.
Cited by (19)
Nasopharyngeal electrodes in temporal lobe epilepsy: A reappraisal of their diagnostic utility
2021, Clinical NeurophysiologyCitation Excerpt :A similar result, that is, superior diagnostic sensitivity of NPE recordings, was obtained for non-lesional TLE. This finding may be supported by studies that have reported interictal spikes more frequently in the mesial temporal lobe than in the lateral temporal lobe on intracranial EEG recordings in patients with non-lesional TLE (Lee et al., 2014, Luther et al., 2011). The pathology and pathophysiological mechanisms of AE are still unclear, and it may be not an uncommon MRI finding in patients with TLE, particularly in patients with a later age of seizure onset (Malter et al., 2016, Na et al., 2020).
Histopathology of 3 Tesla MRI-negative temporal lobe epilepsies
2018, Journal of Clinical NeuroscienceDifferences between mesial and neocortical magnetic-resonance-imaging-negative temporal lobe epilepsy
2016, Epilepsy and BehaviorCitation Excerpt :Despite these findings, it seems that only IEEG is able to provide adequate information about precise SOZ localization, which is essential for surgery. Only a correctly tailored resection can result in seizure freedom in a given patient with a minimal risk of a cognitive decline [14]. If we manage to localize the SOZ correctly in patients with MRI-negative TLE, almost 60% of patients can become seizure-free after the surgery, which is higher than in other types of nonlesional epilepsies and almost comparable to lesional ones.
Yield of non-invasive imaging in MRI-negative focal epilepsy
2024, Journal of Neurology
- 1
Now with University of Arkansas for Medical Sciences, Central Arkansas Veterans Healthcare System, Little Rock, AR, United States.