Preoperative automated fibre quantification predicts postoperative seizure outcome in temporal lobe epilepsy

Keller, Simon S.; Glenn, G. Russell; Weber, Bernd; Kreilkamp, Barbara A.K.; Jensen, Jens Højgaard; Helpern, Joseph A.; Wagner, Jan; Barker, Gareth J.; Richardson, Mark P.; Bonilha, Leonardo

doi:10.1093/brain/aww280

Cited by 105 publications

(104 citation statements)

References 90 publications

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“…Consequently, tractography may provide insight into different patterns of brain damage related to the laterality, type of epilepsy or epileptogenic lesion while along-the-tract analysis of diffusion metrics may also allow extraction of detailed information regarding neuropathology in epilepsy. It may have the potential to identify certain abnormal brain regions in individual patients (Martin et al, 2015), allow inferences about seizure onset zones or may even predict surgical outcomes (Keller et al, 2016). …”

Section: Discussionmentioning

confidence: 99%

Automated tractography in patients with temporal lobe epilepsy using TRActs Constrained by UnderLying Anatomy (TRACULA)

Kreilkamp

Weber

Richardson

et al. 2017

NeuroImage: Clinical

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PurposeA detailed understanding of white matter tract alterations in patients with temporal lobe epilepsy (TLE) is important as it may provide useful information for likely side of seizure onset, cognitive impairment and postoperative prognosis. However, most diffusion-tensor imaging (DTI) studies have relied on manual reconstruction of tract bundles, despite the recent development of automated techniques. In the present study, we used an automated white matter tractography analysis approach to quantify temporal lobe white matter tract alterations in TLE and determine the relationships between tract alterations, the extent of hippocampal atrophy and the chronicity and severity of the disorder.MethodsWe acquired preoperative T1-weighted and DTI data in 64 patients with well-characterized TLE, with imaging and histopathological evidence of hippocampal sclerosis. Identical acquisitions were collected for 44 age- and sex-matched healthy controls. We employed automatic probabilistic tractography DTI analysis using TRActs Constrained by UnderLying Anatomy (TRACULA) available in context of Freesurfer software for the reconstruction of major temporal lobe tract bundles. We determined the factors influencing probabilistic tract reconstruction and investigated alterations of DTI scalar metrics along white matter tracts with respect to hippocampal volume, which was automatically estimated using Freesurfer's morphometric pipelines. We also explored the relationships between white matter tract alterations and duration of epilepsy, age of onset of epilepsy and seizure burden (defined as a function of seizure frequency and duration of epilepsy).ResultsWhole-tract diffusion characteristics of patients with TLE differed according to side of epilepsy and were significantly different between patients and controls. Waypoint comparisons along each tract revealed that patients had significantly altered tissue characteristics of the ipsilateral inferior-longitudinal, uncinate fasciculus, superior longitudinal fasciculus and cingulum relative to controls. Changes were more widespread (ipsilaterally and contralaterally) in patients with left TLE while patients with right TLE showed changes that remained spatially confined in ipsilateral tract regions. We found no relationship between DTI alterations and volume of the epileptogenic hippocampus. DTI alterations of anterior ipsilateral uncinate and inferior-longitudinal fasciculus correlated with duration of epilepsy (over and above effects of age) and age at onset of epilepsy. Seizure burden correlated with tissue characteristics of the uncinate fasciculus.ConclusionThis study shows that TRACULA permits the detection of alterations of DTI tract scalar metrics in patients with TLE. It also provides the opportunity to explore relationships with structural volume measurements and clinical variables along white matter tracts. Our data suggests that the anterior temporal lobe portions of the uncinate and inferior-longitudinal fasciculus may be particularly vulnerable to pathological alterations...

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Section: Discussionmentioning

confidence: 99%

Automated tractography in patients with temporal lobe epilepsy using TRActs Constrained by UnderLying Anatomy (TRACULA)

Kreilkamp

Weber

Richardson

et al. 2017

NeuroImage: Clinical

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“…Each patient underwent a detailed presurgical program, including comprehensive seizure semiology assessment, MRI, neuropsychological assessment, interictal electroencephalography and if clinically necessary, additional invasive electrophysiological recordings, as reported recently 10, 32. All patients showed evidence of a unilateral temporal lobe seizure onset with concomitant ipsilateral HS.…”

Section: Methodsmentioning

confidence: 99%

“…HS was identified by an expert neuroradiologist with considerable experience in lesion diagnosis in epilepsy, which was defined by hippocampal volume loss and internal structure disruption on T1w images, and/or hyperintensities on T2w and FLAIR images 10. There was no evidence of bilateral HS in any patient; all patients had seizures of presumed unilateral temporal lobe origin, and there was no evidence of a secondary extrahippocampal lesion that may have contributed to seizures 32. All patients underwent standardized amygdalohippocampectomy and routine diagnostic analysis of resected hippocampal specimens by an experienced neuropathologist 10.…”

Section: Methodsmentioning

confidence: 99%

Hippocampal subfield segmentation in temporal lobe epilepsy: Relation to outcomes

et al. 2018

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ObjectiveTo investigate the clinical and surgical outcome correlates of preoperative hippocampal subfield volumes in patients with refractory temporal lobe epilepsy (TLE) using a new magnetic resonance imaging (MRI) multisequence segmentation technique.MethodsWe recruited 106 patients with TLE and hippocampal sclerosis (HS) who underwent conventional T1‐weighted and T2 short TI inversion recovery MRI. An automated hippocampal segmentation algorithm was used to identify twelve subfields in each hippocampus. A total of 76 patients underwent amygdalohippocampectomy and postoperative seizure outcome assessment using the standardized ILAE classification. Semiquantitative hippocampal internal architecture (HIA) ratings were correlated with hippocampal subfield volumes.ResultsPatients with left TLE had smaller volumes of the contralateral presubiculum and hippocampus‐amygdala transition area compared to those with right TLE. Patients with right TLE had reduced contralateral hippocampal tail volumes and improved outcomes. In all patients, there were no significant relationships between hippocampal subfield volumes and clinical variables such as duration and age at onset of epilepsy. There were no significant differences in any hippocampal subfield volumes between patients who were rendered seizure free and those with persistent postoperative seizure symptoms. Ipsilateral but not contralateral HIA ratings were significantly correlated with gross hippocampal and subfield volumes.ConclusionsOur results suggest that ipsilateral hippocampal subfield volumes are not related to the chronicity/severity of TLE. We did not find any hippocampal subfield volume or HIA rating differences in patients with optimal and unfavorable outcomes. In patients with TLE and HS, sophisticated analysis of hippocampal architecture on MRI may have limited value for prediction of postoperative outcome.

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“…However, we suggest that there remains the possibility that common structural network alterations may exist in patients with NDfE, and which may be beyond the resolution of VBM. Advanced diffusionbased MRI approaches Glenn et al, 2016;Keller et al, 2017) may provide important insights into structural network alterations in NDfE. Furthermore, a recently published study has shown that pathological structural connectivity causes disturbances to common large-scale functional brain networks regardless of the localization of the epileptogenic zone in patients with refractory focal epilepsy (Besson et al, 2017).…”

Section: Biological and Clinical Implicationsmentioning

confidence: 99%

“…Sophisticated MRI approaches in particular have provided a deeper understanding of the biological mechanisms underlying the development of focal and generalized epilepsies (Bernhardt, Hong, Bernasconi, & Bernasconi, 2013;Duncan, 2005;Koepp & Woermann, 2005), and have recently been used to gain insights into response to surgical intervention in patients with refractory focal epilepsy Keller et al, 2015Keller et al, , 2017Munsell et al, 2015). Sophisticated MRI approaches in particular have provided a deeper understanding of the biological mechanisms underlying the development of focal and generalized epilepsies (Bernhardt, Hong, Bernasconi, & Bernasconi, 2013;Duncan, 2005;Koepp & Woermann, 2005), and have recently been used to gain insights into response to surgical intervention in patients with refractory focal epilepsy Keller et al, 2015Keller et al, , 2017Munsell et al, 2015).…”

Section: Introductionmentioning

confidence: 99%

Resting‐state functional brain networks in adults with a new diagnosis of focal epilepsy

et al. 2018

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ObjectivesNewly diagnosed focal epilepsy (NDfE) is rarely studied, particularly using advanced neuroimaging techniques. Many patients with NDfE experience cognitive impairments, particularly with respect to memory, sustained attention, mental flexibility, and executive functioning. Cognitive impairments have been related to alterations in resting‐state functional brain networks in patients with neurological disorders. In the present study, we investigated whether patients with NDfE had altered connectivity in large‐scale functional networks using resting‐state functional MRI.MethodsWe recruited 27 adults with NDfE and 36 age‐ and sex‐matched healthy controls. Resting‐state functional MRI was analyzed using the Functional Connectivity Toolbox (CONN). We investigate reproducibly determined large‐scale functional networks, including the default mode, salience, fronto‐parietal attention, sensorimotor, and language networks using a seed‐based approach. Network comparisons between patients and controls were thresholded using a FDR cluster‐level correction approach.ResultsWe found no significant differences in functional connectivity between seeds within the default mode, salience, sensorimotor, and language networks and other regions of the brain between patients and controls. However, patients with NDfE had significantly reduced connectivity between intraparietal seeds within the fronto‐parietal attention network and predominantly frontal and temporal cortical regions relative to controls; this finding was demonstrated including and excluding the patients with brain lesions. No common alteration in brain structure was observed in patients using voxel‐based morphometry. Findings were not influenced by treatment outcome at 1 year.ConclusionsPatients with focal epilepsy have brain functional connectivity alterations at diagnosis. Functional brain abnormalities are not necessarily a consequence of the chronicity of epilepsy and are present when seizures first emerge.

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Preoperative automated fibre quantification predicts postoperative seizure outcome in temporal lobe epilepsy

Cited by 105 publications

References 90 publications

Automated tractography in patients with temporal lobe epilepsy using TRActs Constrained by UnderLying Anatomy (TRACULA)

Automated tractography in patients with temporal lobe epilepsy using TRActs Constrained by UnderLying Anatomy (TRACULA)

Hippocampal subfield segmentation in temporal lobe epilepsy: Relation to outcomes

Resting‐state functional brain networks in adults with a new diagnosis of focal epilepsy

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