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Ictal depth EEG and MRI structural evidence for two different epileptogenic networks in mesial temporal lobe epilepsy.

Memarian N, Madsen SK, Macey PM, Fried I, Engel J, Thompson PM, Staba RJ - PLoS ONE (2015)

Bottom Line: MRI analysis found reduced cortical thickness correlated with longer duration of epilepsy.One, identified by HYP ictal onsets, chiefly involves hippocampus and is associated with excellent outcome after standardized anteromedial temporal resection, while the other also involves lateral temporal and orbitofrontal cortex and a seizure-free surgical outcome occurs less after this procedure.These results suggest that a more extensive tailored resection may be required for patients with the second type of MTLE.

View Article: PubMed Central - PubMed

Affiliation: Department of Neurology, David Geffen School of Medicine at UCLA, Los Angeles, CA, United States of America.

ABSTRACT
Hypersynchronous (HYP) and low voltage fast (LVF) activity are two separate ictal depth EEG onsets patterns often recorded in presurgical patients with MTLE. Evidence suggests the mechanisms generating HYP and LVF onset seizures are distinct, including differential involvement of hippocampal and extra-hippocampal sites. Yet the extent of extra-hippocampal structural alterations, which could support these two common seizures, is not known. In the current study, preoperative MRI from 24 patients with HYP or LVF onset seizures were analyzed to determine changes in cortical thickness and relate structural changes to spatiotemporal properties of the ictal EEG. Overall, onset and initial ipsilateral spread of HYP onset seizures involved mesial temporal structures, whereas LVF onset seizures involved mesial and lateral temporal as well as orbitofrontal cortex. MRI analysis found reduced cortical thickness correlated with longer duration of epilepsy. However, in patients with HYP onsets, the most affected areas were on the medial surface of each hemisphere, including parahippocampal regions and cingulate gyrus, whereas in patients with LVF onsets, the lateral surface of the anterior temporal lobe and orbitofrontal cortex showed the greatest effect. Most patients with HYP onset seizures were seizure-free after resective surgery, while a higher proportion of patients with LVF onset seizures had only worthwhile improvement. Our findings confirm the view that recurrent seizures cause progressive changes in cortical thickness, and provide information concerning the structural basis of two different epileptogenic networks responsible for MTLE. One, identified by HYP ictal onsets, chiefly involves hippocampus and is associated with excellent outcome after standardized anteromedial temporal resection, while the other also involves lateral temporal and orbitofrontal cortex and a seizure-free surgical outcome occurs less after this procedure. These results suggest that a more extensive tailored resection may be required for patients with the second type of MTLE.

No MeSH data available.


Related in: MedlinePlus

Radar plot illustrating the results of cluster analysis using anatomical /electrode sites(s) of the SOZ and initial seizure spread.Involvement of each recording site (denoted by radii on each plot) in the SOZ (top row A-C), sites of initial ipsilateral spread (middle row D-F) and initial contralateral spread (bottom row G-I) is expressed as the proportion of total seizures in each cluster (n) indicated by the concentric circles in each plot. Right and left halves of each plot depict medial and lateral aspects respectively of temporal and frontal lobe that included orbitofrontal (OF), amygdala (Am), entorhinal cortex (EC), anterior (AH), middle (MH) and posterior hippocampus (PH), parahippocampal gyrus (PHG), and anterior (a), middle (m), and posterior (p) regions of inferior (ITG) and middle temporal gyri (MTG).
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pone.0123588.g002: Radar plot illustrating the results of cluster analysis using anatomical /electrode sites(s) of the SOZ and initial seizure spread.Involvement of each recording site (denoted by radii on each plot) in the SOZ (top row A-C), sites of initial ipsilateral spread (middle row D-F) and initial contralateral spread (bottom row G-I) is expressed as the proportion of total seizures in each cluster (n) indicated by the concentric circles in each plot. Right and left halves of each plot depict medial and lateral aspects respectively of temporal and frontal lobe that included orbitofrontal (OF), amygdala (Am), entorhinal cortex (EC), anterior (AH), middle (MH) and posterior hippocampus (PH), parahippocampal gyrus (PHG), and anterior (a), middle (m), and posterior (p) regions of inferior (ITG) and middle temporal gyri (MTG).

Mentions: Manual review of depth electrode-recorded seizures found 10 patients who consistently had unilateral HYP onset seizures (Fig 1A) and 14 patients with seizures that regularly began with a LVF ictal onset pattern (Fig 1B). Cluster analysis indicated site(s) of seizure onset (i.e., SOZ) and initial spread were consistent within each patient, but differences were found in the spatial distribution between HYP and LVF onset patterns. Overall, analysis found four clusters of seizures with a mean silhouette value of 0.2 (Fig 2). Eighteen patients (eight HYP, 10 LVF) had seizures that were associated with a single cluster, five patients (two HYP, three LVF) had seizures within two clusters, and one patient (LVF) had seizures among three clusters. The first two clusters consisted of LVF onset seizures only with a diffuse SOZ that involved entorhinal cortex, anterior or middle hippocampus, less frequently amygdala, and differential involvement of posterior hippocampus and parahippocampal gyrus, anterior aspects of middle and inferior temporal gyri, and orbitofrontal cortex (Fig 2A). By contrast, the third cluster contained HYP onset seizures only with a SOZ that chiefly involved anterior hippocampus and less frequently parahippocampal gyrus (Fig 2B). The fourth cluster contained LVF onset seizures that involved fewer sites in the SOZ compared to the first two clusters of this same EEG onset pattern (Fig 2C), but also contained HYP onset seizures that had a SOZ similar to the LVF onset seizures in this cluster (Fig 2C). Overall, compared to HYP onset seizures, LVF onset seizures first appeared on a significantly greater number of electrodes and were more likely to be recorded simultaneously in multiple mesial temporal lobe sites as well as lateral temporal and orbitofrontal cortex (Tables 1 and 2).


Ictal depth EEG and MRI structural evidence for two different epileptogenic networks in mesial temporal lobe epilepsy.

Memarian N, Madsen SK, Macey PM, Fried I, Engel J, Thompson PM, Staba RJ - PLoS ONE (2015)

Radar plot illustrating the results of cluster analysis using anatomical /electrode sites(s) of the SOZ and initial seizure spread.Involvement of each recording site (denoted by radii on each plot) in the SOZ (top row A-C), sites of initial ipsilateral spread (middle row D-F) and initial contralateral spread (bottom row G-I) is expressed as the proportion of total seizures in each cluster (n) indicated by the concentric circles in each plot. Right and left halves of each plot depict medial and lateral aspects respectively of temporal and frontal lobe that included orbitofrontal (OF), amygdala (Am), entorhinal cortex (EC), anterior (AH), middle (MH) and posterior hippocampus (PH), parahippocampal gyrus (PHG), and anterior (a), middle (m), and posterior (p) regions of inferior (ITG) and middle temporal gyri (MTG).
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4388829&req=5

pone.0123588.g002: Radar plot illustrating the results of cluster analysis using anatomical /electrode sites(s) of the SOZ and initial seizure spread.Involvement of each recording site (denoted by radii on each plot) in the SOZ (top row A-C), sites of initial ipsilateral spread (middle row D-F) and initial contralateral spread (bottom row G-I) is expressed as the proportion of total seizures in each cluster (n) indicated by the concentric circles in each plot. Right and left halves of each plot depict medial and lateral aspects respectively of temporal and frontal lobe that included orbitofrontal (OF), amygdala (Am), entorhinal cortex (EC), anterior (AH), middle (MH) and posterior hippocampus (PH), parahippocampal gyrus (PHG), and anterior (a), middle (m), and posterior (p) regions of inferior (ITG) and middle temporal gyri (MTG).
Mentions: Manual review of depth electrode-recorded seizures found 10 patients who consistently had unilateral HYP onset seizures (Fig 1A) and 14 patients with seizures that regularly began with a LVF ictal onset pattern (Fig 1B). Cluster analysis indicated site(s) of seizure onset (i.e., SOZ) and initial spread were consistent within each patient, but differences were found in the spatial distribution between HYP and LVF onset patterns. Overall, analysis found four clusters of seizures with a mean silhouette value of 0.2 (Fig 2). Eighteen patients (eight HYP, 10 LVF) had seizures that were associated with a single cluster, five patients (two HYP, three LVF) had seizures within two clusters, and one patient (LVF) had seizures among three clusters. The first two clusters consisted of LVF onset seizures only with a diffuse SOZ that involved entorhinal cortex, anterior or middle hippocampus, less frequently amygdala, and differential involvement of posterior hippocampus and parahippocampal gyrus, anterior aspects of middle and inferior temporal gyri, and orbitofrontal cortex (Fig 2A). By contrast, the third cluster contained HYP onset seizures only with a SOZ that chiefly involved anterior hippocampus and less frequently parahippocampal gyrus (Fig 2B). The fourth cluster contained LVF onset seizures that involved fewer sites in the SOZ compared to the first two clusters of this same EEG onset pattern (Fig 2C), but also contained HYP onset seizures that had a SOZ similar to the LVF onset seizures in this cluster (Fig 2C). Overall, compared to HYP onset seizures, LVF onset seizures first appeared on a significantly greater number of electrodes and were more likely to be recorded simultaneously in multiple mesial temporal lobe sites as well as lateral temporal and orbitofrontal cortex (Tables 1 and 2).

Bottom Line: MRI analysis found reduced cortical thickness correlated with longer duration of epilepsy.One, identified by HYP ictal onsets, chiefly involves hippocampus and is associated with excellent outcome after standardized anteromedial temporal resection, while the other also involves lateral temporal and orbitofrontal cortex and a seizure-free surgical outcome occurs less after this procedure.These results suggest that a more extensive tailored resection may be required for patients with the second type of MTLE.

View Article: PubMed Central - PubMed

Affiliation: Department of Neurology, David Geffen School of Medicine at UCLA, Los Angeles, CA, United States of America.

ABSTRACT
Hypersynchronous (HYP) and low voltage fast (LVF) activity are two separate ictal depth EEG onsets patterns often recorded in presurgical patients with MTLE. Evidence suggests the mechanisms generating HYP and LVF onset seizures are distinct, including differential involvement of hippocampal and extra-hippocampal sites. Yet the extent of extra-hippocampal structural alterations, which could support these two common seizures, is not known. In the current study, preoperative MRI from 24 patients with HYP or LVF onset seizures were analyzed to determine changes in cortical thickness and relate structural changes to spatiotemporal properties of the ictal EEG. Overall, onset and initial ipsilateral spread of HYP onset seizures involved mesial temporal structures, whereas LVF onset seizures involved mesial and lateral temporal as well as orbitofrontal cortex. MRI analysis found reduced cortical thickness correlated with longer duration of epilepsy. However, in patients with HYP onsets, the most affected areas were on the medial surface of each hemisphere, including parahippocampal regions and cingulate gyrus, whereas in patients with LVF onsets, the lateral surface of the anterior temporal lobe and orbitofrontal cortex showed the greatest effect. Most patients with HYP onset seizures were seizure-free after resective surgery, while a higher proportion of patients with LVF onset seizures had only worthwhile improvement. Our findings confirm the view that recurrent seizures cause progressive changes in cortical thickness, and provide information concerning the structural basis of two different epileptogenic networks responsible for MTLE. One, identified by HYP ictal onsets, chiefly involves hippocampus and is associated with excellent outcome after standardized anteromedial temporal resection, while the other also involves lateral temporal and orbitofrontal cortex and a seizure-free surgical outcome occurs less after this procedure. These results suggest that a more extensive tailored resection may be required for patients with the second type of MTLE.

No MeSH data available.


Related in: MedlinePlus