Imaging structure and function in refractory focal epilepsy

doi:10.1016/S1474-4422(04)00965-2

The Lancet Neurology

Volume 4, Issue 1, January 2005, Pages 42-53

https://doi.org/10.1016/S1474-4422(04)00965-2 Get rights and content

Summary

Over the past decade there have been many advances in data acquisition and analysis for structural and functional neuroimaging of people with epilepsy. New imaging sequences and analysis techniques have increased the resolution of images such that underlying structural pathology can be seen in many patients with “cryptogenic” epilepsy. When an epileptogenic lesion is present, antiepileptic drugs alone rarely prevent seizures. However, the success of surgical treatment is improved when a structural lesion has been identified. Lesions might not overlap with the area of the cortex generating seizures and may continue into areas sustaining normal functions. To prevent postsurgical morbidity, the spatial relation between functionally important areas and the epileptogenic lesion must be assessed before surgery. In this review we describe the potential of different neuroimaging techniques to show lesions, assess neuronal function, and assist with the prognosis of postsurgical outcome in patients with refractory focal epilepsy.

Section snippets

Imaging methods

MRI is generally the imaging technique of choice for identifying the structural basis of the epilepsies. Functional MRI (fMRI), PET, or single-photon-emission CT (SPECT) assess cerebral function and functional impairment. Identification of chemical processes and receptor systems is mainly restricted to research with PET and magnetic resonance spectroscopy.

Two types of imaging studies are important in the clinical assessment of patients: firstly, averaging of many patients' measurements,

Integration of EEG and imaging

The epileptogenic zone is the area of cortex necessary for seizure generation.⁶ Because the epileptogenic zone is a theoretical concept, there is no technique to measure it directly, and previously unidentified epileptogenic zones could present postsurgery.⁶

The location of the epileptogenic zone can be inferred through identification of the epileptogenic lesion with MRI or PET data, and its relation to the seizure-onset and irritative zone. The area of seizure onset might be the same or smaller

Defining the causes of focal epilepsies

Underlying structural pathology can be found in most patients with focal epilepsies; 74% of those assessed at tertiary referral centres had abnormal MRI,⁷ and structural abnormality was found in about 50% of those assessed in the community.⁸ Table 1 shows the appropriate MRI sequences for the most common pathologies.

Hippocampal sclerosis

The most common pathology in refractory partial seizure disorders is hippocampal sclerosis, found in about 32% of patients with chronic disorders,⁷ but in only 1–3% of patients with newly diagnosed partial epilepsy.9, 10 Mesial-temporal-lobe epilepsy due to unilateral hippocampal sclerosis is the prototype focal epilepsy syndrome remediable through surgery.¹¹

MRI in patients with temporal-lobe epilepsy

Experienced neuroradiologists are able to visually diagnose hippocampal atrophy in 80–90% of histologically verified cases. Quantitative MRI measurements of hippocampal volumes¹² or hippocampal T213, 14 relaxation times only marginally increase the sensitivity to 90–95% (figure 1).¹⁵ These MRI measurements are essential in research, and in clinical practice they complement each other by identifying either subtle unilateral or bilateral hippocampal sclerosis in certain patients.¹⁶ New

PET and SPECT in patients with temporal-lobe epilepsy

In mesial-temporal-lobe epilepsy, fluorine-18-labelled-deoxyglucose PET typically measures widespread interictal hypometabolism, the pathophysiology of which is incompletely understood. Atrophy has a major effect on cerebral metabolism,²⁶ but interictal hypometabolism might reflect the preferential networks involved by ictal discharges and pathways of seizure spread.27, 28 Contralateral dystonic posturing was associated with both interictal hypometabolism²⁹ and increased ictal cerebral blood

“MRI-negative” patients

In about 20% of patients with chronic focal epilepsies, pathology is not seen on visual inspection of high resolution MRI.2, 7 Imaging research is directed at such patients.

Malformation of cortical development

The second most common cause of refractory epilepsy in adults is malformation of cortical development.⁸² High-resolution MRI, ideally with multiplanar study, is needed for diagnosis of malformation of cortical development with imaging. Routine MRI cannot detect or identify the extent of all pathologies. Freedom from seizures after surgery is closely related to resection of the whole malformation of cortical development;83, 84 identification of widespread or bilateral changes typically excludes

Tumours

Benign tumours commonly underlie refractory partial seizures. About 20% of adults and children who had surgery for chronic epilepsy had a benign tumour, most commonly in the temporal lobe. Gangliogliomas and dysembryoplastic neuroepithelial tumours are benign developmental glial-neuronal tumours that cause focal epilepsy with onset before age 20 years. They are classified as benign because they typically lack mass effect and are stable on serial imaging.¹⁰⁶ Complete resection of

Effect of focal epilepsy on cognitive function

fMRI provides a measure of brain activity during cognitive processes by contrasting concentrations of oxygen in the blood.¹¹³ Various tasks may be done during fMRI to target specific cortical networks. Task-related blood-oxygenation-level-dependent changes are subtle, a few percent at 1·5 tesla.¹¹⁴ fMRI relies heavily on the tasks used and the assumptions that underlie them.¹¹⁵ The design of the tasks needs to be tailored so that patients can do them. Studies in which there is little or no

Language

During linguistic tasks fMRI readily and reliably identifies the language-dominant hemisphere. fMRI-language tests and the Wada test are 90% concordant for identification of the hemisphere dominant for language. Partial disparity occurs in 10% of patients, and overt discordance is rare but may occur under recognisable circumstances. A recent report, in which patients silently generated words beginning with a certain letter, suggests that fMRI may be less reliable in lateralising language

Localisation of language

fMRI activation in areas without disruption of function on electrocortical stimulation is common. These false positive fMRI activations are not surprising because networks of regions are activated with this technique and some are not essential for the task in question. Regions showing disruption by electrocortical stimulation but no fMRI activations are critical when planning a surgical resection. In comparison with electrocortical stimulation, fMRI showed a high predictive power for the

Evidence of reorganisation

A high proportion (33%) of patients with left-temporal-lobe epilepsy show bilateral or right hemisphere language-related lateralisation, suggesting plasticity of language representation in the brains of many patients with intractable temporal-lobe epilepsy.¹²⁴ A semantic decision task compared with a non-linguistic decision task showed atypical or weak language dominance in about 20% of patients.125, 126 Silent word generation tasks mostly activate the frontal cortex and not the anterior

Memory

The main purpose of preoperative neuropsychological testing is to predict postoperative functional impairment and possible neuropsychological rehabilitation. The Wada test is primarily used to assess adequate postoperative function in the temporal lobe contralateral to the hemisphere involved in surgery; it does not reliably indicate impairment of verbal memory after surgery to the language-dominant temporal lobe. Assessment of hippocampal integrity to sustain memory is critical for planning

Verbal memory

A linguistic encoding task¹³⁴ indicated the hemisphere of seizure focus in patients with temporal-lobe epilepsy. Activations on fMRI were unilateral in healthy controls, increased in the left hippocampus and parahippocampal gyrus in patients with right-temporal-lobe epilepsy, but reduced in the left hippocampus in patients with left-temporal-lobe epilepsy. A verbal-memory encoding task was associated with a similar reorganisation from left to right hippocampus and parahippocampal gyrus in

Non-verbal memory

A semantic decision task¹³⁷ produced bilateral and broadly symmetrical mesial-temporal-lobe activations in controls but in patients with temporal-lobe epilepsy the activation was asymmetric. fMRI activations were mostly consistent with the results of the Wada test, particularly in patients with good performance, though lateralisation was seen even in patients who performed poorly on the recognition task. A visuospatial task¹³⁸—patients were asked to imagine a walk through their home

Prediction of postsurgical memory

Meaningful data are needed for individual patients for fMRI to be part of the presurgical assessment—so far this has proved difficult. Recent studies suggest a predictive value of fMRI for postsurgical memory outcome. Rabin and colleagues¹⁴⁰ used a complex visual scene-encoding task, that causes symmetrical mesial- temporal-lobe activation in controls, to show a relation between mesial-temporal-lobe activation asymmetry ratios and postsurgical memory outcome; increased activation ipsilateral to

Functional connectivity

The activity maps produced from neuroimaging studies suggest that cognitive functions arise from the action of distributed networks in the brain. On the basis of meticulous investigations with multiple depth-electrodes in patients with epilepsy, Bancaud and Talairach¹⁴² emphasised a similar concept of interconnected regions composed of a pacemaker and relay and subrelay areas essential for producing individual ictal symptoms and signs. Corticocortical facilitatory connections allow propagation

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ReviewImaging structure and function in refractory focal epilepsy

Summary

Section snippets

Imaging methods

Integration of EEG and imaging

Defining the causes of focal epilepsies

Hippocampal sclerosis

MRI in patients with temporal-lobe epilepsy

PET and SPECT in patients with temporal-lobe epilepsy

“MRI-negative” patients

Malformation of cortical development

Tumours

Effect of focal epilepsy on cognitive function

Language

Localisation of language

Evidence of reorganisation

Memory

Verbal memory

Non-verbal memory

Prediction of postsurgical memory

Functional connectivity

Lancet

Epilepsy Res

Neuroimage

Neuroimage

Epilepsy Res

Neuroimage

Epilepsy Res

Magn Reson Imaging

Lancet Neurol

Neuroimage

Neuroimage

Magn Reson Imaging

Is the underlying cause of epilepsy a major prognostic factor for recurrence?

Neurology

A randomized, controlled trial of surgery for temporal-lobe epilepsy

N Engl J Med

Seizure outcome after epilepsy surgery in children and adolescents

Ann Neurol

Long-term outcome after epilepsy surgery for focal cortical dysplasia

J Neurosurg

Temporal lobe epilepsy: analysis of patients with dual pathology

Acta Neurol Scand

Presurgical evaluation of epilepsy

Brain

High resolution magnetic resonance imaging in adults with partial or secondary generalised epilepsy attending a tertiary referral unit

J Neurol Neurosurg Psychiatry

Progressive neocortical damage in epilepsy

Ann Neurol

The structural consequences of newly diagnosed seizures

Ann Neurol

Temporal lobe seizures: lateralization with MR volume measurements of the hippocampal formation

Radiology

Detection of hippocampal pathology in intractable partial epilepsy: increased sensitivity with quantitative magnetic resonance T2 relaxometry

Neurology

Regional changes in hippocampal T2 relaxation and volume: a quantitative magnetic resonance imaging study of hippocampal sclerosis

J Neurol Neurosurg Psychiatry

A systematic approach for interpreting MR images of the seizure patient

Am J Roentgenol

Frequency and characteristics of dual pathology in patients with lesional epilepsy

Neurology

Mesial temporal damage in temporal lobe epilepsy: a volumetric MRI study of the hippocampus, amygdala and parahippocampal region

Brain

Medial temporal lobe atrophy in patients with refractory temporal lobe epilepsy

J Neurol Neurosurg Psychiatry

Entorhinal cortex MRI assessment in temporal, extratemporal, and idiopathic generalized epilepsy

Epilepsia

MRI volumetry of the thalamus in temporal, extratemporal, and idiopathic generalized epilepsy

Neurology

Extratemporal atrophy in patients with complex partial seizures of left temporal origin

Ann Neurol

Extrahippocampal temporal lobe atrophy in temporal lobe epilepsy and mesial temporal sclerosis

Brain

Magnetic resonance spectroscopy in temporal lobe epilepsy

Neurology

In vivo hippocampal glucose metabolism in mesial temporal lobe epilepsy

Neurology

Metabolic changes and electro-clinical patterns in mesio-temporal lobe epilepsy: a correlative study

Brain

Insular cortex involvement in mesiotemporal lobe epilepsy: a positron emission tomography study

Review
Imaging structure and function in refractory focal epilepsy