Journal of Medical Imaging and Radiation Oncology •• (2014) ••–•• bs_bs_banner
R ADIOLO GY—PI CTO R I AL E SSAY
Magnetic resonance imaging in adults with epilepsy: A pictorial essay Jolandi van Heerden,1 Patricia M. Desmond,1 Brian M. Tress,1 Patrick Kwan,2 Terence J. O’Brien2 and Elaine H. Lui1 1 Department of Radiology and 2Departments of Medicine and Neurology, The Royal Melbourne Hospital, The University of Melbourne, Melbourne, Victoria, Australia
J van Heerden MBChB, MMed (radiology), FRANZCR; PM Desmond MSc MDBS FRANZCR; BM Tress MDBS FRANZCR FRCR; P Kwan BMedSci, MBBBC, FRACP, PhD; TJ O’Brien MBBS, FRACP; EH Lui MBBS, MMed (radiology), FRANZCR. Correspondence Dr Jolandi van Heerden, Department of Radiology, The Royal Melbourne Hospital, 300 Grattan Street, Parkville, Melbourne, Vic. 3050, Australia. Email: [email protected]
Summary This pictorial essay highlights the role of the radiologist as a member of the adult epilepsy multidisciplinary team, and gives an overview of MRI-evident epileptogenic lesions. Key words: adult neuroradiology.
neuroimaging;
magnectic
resonance
imaging;
Conflict of interest: None of the authors have conflicts of interest to declare. Disclaimer: No funding was received for this pictorial essay. All the images have been anonymised and were collected retrospectively. Submitted 28 November 2013; accepted 07 December 2013. doi:10.1111/1754-9485.12150
Background Epilepsy is a chronic neurologic condition characterised by recurrent epileptic seizures as clinical manifestations of abnormal, excessive neuronal activity, affecting 0.5–1% of the world population.1 The diagnosis and management of patients with epilepsy have evolved into a multidisciplinary team approach involving neurologists sub-specialised as epileptologists, neurosurgeons, neuropsychiatrists, neuropsychologists, social workers, specialist nurses, counsellors, nuclear medicine physicians and radiologists.1 The primary role of a radiologist is to assess for the presence of structural abnormalities that may be a cause of the epilepsy. Magnetic resonance imaging (MRI) is © 2014 The Royal Australian and New Zealand College of Radiologists
currently the structural imaging modality of choice. Magnetic resonance imaging in combination with clinical assessment, electroencephalography, single-photon emission computed tomography and/or positron emission tomography aid with diagnosis and management. In treatment-refractory cases where multidisciplinary clinical, radiological, nuclear medicine and electrophysiological findings are concordant, surgical resection of a focal epileptogenic lesion situated in a non-eloquent brain region can be considered. In this context, the radiologist can further assist with preoperative planning. Seizure classification is complex and evolving and can be classified by mode of seizure onset (generalised/ focal), aetiology (genetic, structural/metabolic, unknown) or by syndromes.2 Although the precise 1
J van Heerden et al.
terminology is under revision, the clinical importance of whether there is impairment of awareness during a seizure is well recognised. Structural lesions identifiable by MRI often (but not always) present with focal epilepsy and knowledge of typical seizure symptoms and signs can help target the search for a subtle structural lesion (Table 1).1 For instance, focal onset seizures associated with impaired awareness most frequently emanate from the temporal lobe, where the commonest associated structural abnormality is mesial temporal sclerosis (MTS). However, a structural potentially epileptogenic lesion may not be the cause of a patient’s epilepsy, and correlation with clinical, electroencephalography and/or other nuclear medicine imaging findings is essential. Utilisation of a targeted epilepsy protocol will optimise the detection of subtle lesions. Recently, an ‘essential 6’ sequence protocol has been suggested that includes volumetric T1WI, thin-section two-plane fluidattenuated inversion recovery and T2WI (angled to the hippocampi) as well as a haemosiderin/calcificationsensitive sequence.3
a
c
Table 1. Typical seizure symptoms related to various regions of the brain1 Likely location of epileptogenic focus Frontal lobe Mesial temporal lobe
Supplementary motor cortex Motor cortex Sensory cortex
Occipital lobe
Symptoms and signs
Bizarre complex behaviour Forced eye deviation Odd smell Feelings of fear Butterflies in stomach Deja vú Depersonalisation experiences Fencer posturing Focal tonic limb movement Paresthesias Numbness Pain (rare) False sense of inability to move limb Haemianopia Flashing lights Visual distortion Subjective feeling of eye movement Visual hallucination (rare) Nystagmus (rare)
b
d
e
Fig. 1. Mesial temporal sclerosis (MTS). (a) Thin section coronal T2WI MRI showing typical left mesial temporal sclerosis (thick white arrow). The left hippocampus has a reduced volume, loss of internal architectural definition and increased signal. (b) Coronal fluid-attenuated inversion recovery MRI in a different patient demonstrating loss of grey–white matter differentiation in the right anterior temporal lobe with increased signal, often associated with ipsilateral MTS/temporal lobe epilepsy. (c) and (d) Preoperative functional MRI (fMRI) in a patient with left-sided MTS showing ipsilateral language dominance with dominant left Wernicke’s area activation (long white arrow in d) and bilateral Broca’s area activation (short white arrows in c). (e) Post-hippocampectomy sagittal T1WI shows a small volume residual hippocampal posterior body and tail (white arrow).
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© 2014 The Royal Australian and New Zealand College of Radiologists
MRI in adults with epilepsy
Fig. 2. Right amygdala dysplasia. Coronal T2WI MRI shows enlargement with increased signal of the right amygdala (black arrow). Amygdala dysplasia was confirmed histopathologically.
Mesial temporal sclerosis Mesial temporal sclerosis is the commonest epileptogenic abnormality detected on MRI in patients with drugresistant focal epilepsy.4 Well-planned and executed surgical resection in appropriately selected patients with MTS has a good prognosis for long-term seizure control.5 High-resolution coronal T2WI sequences angled to the hippocampi are needed to optimally evaluate for the characteristic changes of MTS, namely increased T2WI signal, reduced volume and loss of architecture in the affected hippocampus (Fig. 1a).4,6 In addition, loss of the
a
b
Fig. 3. Normal variation. Coronal T2WI MRI shows incomplete inversion of the left hippocampus. The left hippocampus is more rounded and vertically orientated with preserved signal. In this case, the internal hippocampal architecture is preserved; however, in some cases, mild blurring may be observed. The adjacent collateral sulcus is vertically orientated (thick white arrow) with resultant irregular shape of the left ventricular temporal horn (black arrow). The left fornix is inferiorly displaced (thin white arrow).
gray–white matter differentiation in the ipsilateral anterior temporal lobe is seen in up to 58% of patients with drug-resistant temporal lobe epilepsy and 64% of patients with MTS (Fig. 1b).7 Less frequently, ipsilateral
c
Fig. 4. Developmental abnormalities. (a) Coronal fluid-attenuated inversion recovery MRI shows type IIb focal cortical dysplasia involving the right superior frontal sulcus with a characteristic ‘transmantle sign’ (thin white arrow) in a patient with other remote left parietal and left temporal regions of trauma-related cortical injury (thick white arrows). (b) Volumetric coronal T1WI MRI shows left parietal polymicrogyria with small irregular gyri and thickened cortex (black arrow). (c) Volumetric axial T1WI MRI demonstrates complex cortical migration and organisation abnormalities with right temporal polymicrogyria (thick black arrow), right temporal closed lip schizencephaly (thin black arrow), as well as abnormal gyration and morphology of the right hippocampus (white arrows). © 2014 The Royal Australian and New Zealand College of Radiologists
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Fig. 5. Grey matter heterotopia. (a) Volumetric coronal T1WI MRI shows extensive bi-hemispheric subcortical grey matter band heterotopia (black arrows). (b) Coronal T2WI shows a tiny focus of periventricular nodular grey matter heterotopia along the roof of the right temporal horn (white arrow).
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Fig. 6. Sturge Weber syndrome. (a) Axial contrast-enhanced T1WI MRI demonstrates enhancing left occipital pial angiomatosis (white arrows). (b) Axial T2WI shows left hemispheric atrophy. (c) Susceptibility weighted imaging sequence shows angiomatosis with cortical mineralisation (white arrows). Imaging findings correlated with the clinically evident cutaneous ‘port wine stain’.
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b
c
Fig. 7. Tuberous Sclerosis. Imaging in a patient with worsening seizures in the context of known tuberous sclerosis previously lost to follow-up demonstrating an interval left frontal high grade glioma. (a) Axial fluid-attenuated inversion recovery MRI shows typical imaging findings related to tuberous sclerosis with left occipital subcortical tubers (short thick black arrow) and right frontal radial glial bands (long thin black arrows) as well as left periventricular sub-ependymal nodules (white arrows). (b) and (c) Coronal contrast-enhanced T1WI MRI and axial MRI cerebral blood volume (CBV) perfusion map demonstrate an interval heterogeneously enhancing left frontal high-grade glial tumour with cortical extension (thick black arrows).
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© 2014 The Royal Australian and New Zealand College of Radiologists
MRI in adults with epilepsy
Fig. 8. Low-grade tumours – histopathologically confirmed. (a) Axial fluid-attenuated inversion recovery MRI shows a non-enhancing low-grade glioma involving the left uncus and amygdala (white arrow). (b) Coronal T2WI MRI demonstrates a dysembioplastic neuroepithelial tumour involving the cornu ammonis (CA1–3) of the right hippocampus (white arrow). (c) Coronal contrast enhanced T1WI shows a ganglioglioma with enhancing (black arrow) and non-enhancing cystlike (white arrow) components involving the left para-hippocampal gyrus and fusiform gyrus.
Fig. 9. Extra-axial tumours causing seizures. (a) Coronal T2WI MRI shows a craniopharyngioma with heterogeneous sellar and supra-sellar proteinaceous cyst-like components impressing on the left mesial temporal lobe (white arrow) that correlated with electroencephalography (EEG) findings. (b) Coronal contrast-enhanced T1WI MRI shows a right fronto-parietal meningioma (white arrow) with adjacent cortical and subcortical signal change (black arrow) with EEG correlation.
Fig. 10. Traumatic brain injury. (a) Axial T2WI MRI shows bi-frontal cortical and subcortical encephalomalacia (white arrows) with ex-vacuo dilatation of the right ventricular frontal horn. (b) MRI susceptibility weighted imaging in the same patient shows trauma-related blood product deposition along the genu and splenium of the corpus callosum (black arrows) as well as bi-frontal cortical superficial siderosis (white arrows).
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© 2014 The Royal Australian and New Zealand College of Radiologists
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fornix and mamillary body atrophy can also be seen.4,6 Bilateral MTS is not uncommon, and there is a known association between MTS and a second epileptogenic lesion, particularly cortical dysgenesis, necessitating careful assessment of the adjacent cortex and amygdala as well as the contralateral hippocampus.4 Altered amygdala signal with volume increase raises the possibility of amygdala dysplasia (Fig. 2) or tumour4 (with post-ictal change a differential), whereas volume loss suggests amygdala sclerosis.6 Preoperative lateralisation of language dominance with functional MRI (Fig. 1c,d) can complement preoperative neuropsychology assessment. A modified partial
a
b
d
e
mesiotemporal resection can be considered in MTS ipsilateral to the side of language dominance to reduce the risk of post-surgical memory-related word-finding difficulty.8 Following hippocampectomy, it is important to comment on the amount of residual hippocampus as well as the extent of post-surgical gliosis to guide decision making if further surgery is considered in the context of seizure recurrence (Fig. 1e). One potential pitfall to be aware of is incomplete hippocampal inversion – a non-epileptogenic congenital variant found in approximately 19% of the general population (Fig. 3).9
c
f
Fig. 11. Infection. (a–c) Axial contrast-enhanced T1WI, diffusion-weighted imaging and apparent diffusion coefficient map show a left occipital rim-enhancing, centrally restricting bacterial abscess (white arrows) with intra-ventricular breakthrough (black arrows). (d) Axial T2WI MRI shows right temporal encephalomalacia as a late consequence of herpes simplex virus encephalitis. (e–f) Axial T2WI MRI and coronal contrast-enhanced T1WI demonstrating the colloidal vesicular stage of neurocysticercosis involving the right anterior temporal pole with marked peri-lesional inflammatory reaction (black arrow in e) and lesional rim enhancement as well as dot-like enhancement of the scolex (white arrow in f).
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© 2014 The Royal Australian and New Zealand College of Radiologists
MRI in adults with epilepsy
with established diagnoses, follow-up imaging should evaluate for interval change (Fig. 7).
Developmental abnormalities Abnormalities of cortical migration and organisation can be subtle and should be carefully searched for using high-resolution volumetric imaging with multi-planar reconstructions. Focal cortical dysplasia (FCD) results from abnormal focal cortical organisation and is categorised into three types on histopathology.10 FCD is classically detected with grey–white matter junction blurring and abnormal subjacent white matter signal.10 Type I is classically associated with focal hypoplasia (‘deep sulcus sign’).10 Type IIb (Taylor’s type with balloon cells) is commonly associated with subcortical white matter hyperintensity tapering towards the ventricle (‘transmantle sign’) (Fig. 4a) best appreciated on T2WI and fluid-attenuated inversion recovery sequences.10 Polymicrogyria and schizencephaly are caused by abnormalities in neuronal migration and cortical organisation and have characteristic radiological appearances (Fig. 4b,c).11 Grey matter heterotopia relates to arrested or disrupted migration of groups of neurons from periventricular germinal zone to cortex and can manifest as periventricular nodular heterotopias, band heterotopias or nodular subcortical heterotopias (Fig. 5).11 In the adult population, the diagnosis of congenital phakomatoses such as tuberous sclerosis and Sturge Weber syndrome (Fig. 6) causing epilepsy is often already established, but occasionally, radiologists may still be the first to suggest these conditions. In patients
a
b
Tumours In young adults with epilepsy, particular tumours to consider include ganglioglioma, dysembryoplastic neuroepithelial tumour (DNET), pleomorphic xanthoastrocytoma (PXA), pilocytic astrocytoma, low-grade glioma and oligodendroglioma (Fig. 8).12 Tumours can have associated FCD (FCD IIIb); thus, peri-tumoural cortex should also be carefully examined.10,11 In the older adult population, high-grade gliomas (Fig. 7b,c), metastases and other rarer tumours that classically involve dural surfaces such as gliosarcomas should be considered.12 Extra-axial tumours can also cause seizures (Fig. 9).12
Trauma Traumatic brain injury resulting in contusions, extraaxial haemorrhages or diffuse axonal injury has a high incidence of both early- and late-onset seizures (Fig. 10).13
Infection Focal seizures can be caused by meningitis but are particularly associated with instances of focal viral or bacterial cerebritis or abscess formation2 (Fig. 11a–d). Atypical organisms such as neurocysticercosis and
c
Fig. 12. Vascular lesions. (a) Axial T2WI MRI shows a right parietal arteriovenous malformation (white arrow) with a superficial nidus involving cortex. (b) Axial T2WI MRI shows the characteristic ‘pop corn’ appearance of two cavernomas involving the right cerebral peduncle (thick white arrow) and right mesial temporal lobe (thin white arrow) with associated circumferential haemosiderin blooming (c) Volumetric axial contrast-enhanced T1WI MRI show developmental venous anomalies (black arrows) associated with the cavernomas shown in (b). © 2014 The Royal Australian and New Zealand College of Radiologists
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tuberculosis can be epileptogenic in all disease phases (Fig. 11e,f).
Vascular Supra-tentorial cerebral vascular malformations most frequently associated with epilepsy are cavernomas and arteriovenous malformations (AVMs), particularly when involving cortex and the temporal lobes (Fig. 12).14 Cavernomas are benign, angiographically occult lesions consisting of intertwined clusters of sinusoidal vascular channels.14 AVMs represent a cluster/nidus of directly communicating arteries and veins without an intervening capillary network.14 Based on size, location and drainage, AVMs are classified using the Spetzler–Martin system for the purposes of surgical prognostication.14 Haemorrhage as a complication in both AVMs and cavernomas can result in seizures even in previously asymptomatic lesions.14 Epileptic seizures can develop as an early or late consequence of both arterial and venous cortical infarcts.15
Conclusion This pictorial essay highlights the radiologist’s role in the adult epilepsy multidisciplinary team and reviews MRIevident epileptogenic lesions that should be considered.
References 1. Fisher RS, Stein A, Karls J. Epilepsy for the Neuroradiologist. AJNR 1997; 18: 851–63. 2. Berg AT, Berkovic SF, Brodie MJ, Buchhalter J, Cross JH et al. Revised terminology and concepts for organization of seizures and epilepsies: report of the ILAE Commission on Classification and Terminology. Epilepsia 2010; 51: 676–85. 3. Wellmer J, Quesada CM, Rothe L, Elger CE, Bien CG, Urbach H. Proposal for a magnetic resonance imaging protocol for the detection of epileptogenic lesions at early outpatient stages. Epilepsia 2013; 54: 1977–87. 4. Malmgren K, Thom M. Hippocampal sclerosis – origins and imaging. Epilepsia 2012; 53 (Suppl 4): 19–33.
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5. Lowe A, David E, Kilpatrick C, Matkovic Z, Cook M, Kaye A, O’Brien TJ. Epilepsy surgery for pathologically proven hippocampal sclerosis provides long term seizure control and improved quality of life. Epilepsia 2004; 45: 237–42. 6. Chan S, Erickson JK, Yoon SS. Limbic system abnormalities associated with mesial temporal sclerosis: a model of chronic cerebral changes due to seizures. Radiographics 1997; 17: 1095–110. 7. Mitchell LA, Jackson GD, Kalnins RM, Saling MM, Fitt GJ et al. Anterior temporal abnormality in temporal lobe epilepsy: a quantitative MRI and histopathologic study. Neurology 1999; 52: 327–36. 8. Mintzer S, Sperling MR. When should a resection sparing mesial structures be considered for temporal lobe epilepsy? Epilepsy Behav 2008; 13: 7–11. 9. Bajic D, Wang C, Kumlien E, Mattsson P, Lundberg S, Eeg-Olofsson O, Raininko R. Incomplete inversion of the hippocampus – a common developmental anomaly. Eur Radiol 2008; 18: 138–42. 10. Colombo N, Tassi L, Galli C, Citterio A, Russo GL et al. Focal cortical dysplasias: MR Imaging, histopathologic, and clinical correlations in surgically treated patients with epilepsy. AJNR 2003; 24: 724–33. 11. Shorvon SD, Andermann F, Guerrini R (2011) The Causes of Epilepsy: Common and Uncommon Causes in Adults and Children. Cambridge University Press, Cambridge. 12. Beaumont A, Whittle IR. The pathogenesis of tumour associated epilepsy. Acta Neurochir (Wien) 2000; 142: 1–15. 13. Kazemi H, Hashemi-Fesharaki S, Razaghi S, Najafi M, Kolivand PH et al. Intractable epilepsy and craniocerebral trauma: analysis of 163 patients with blunt and penetrating head injuries sustained in war. Injury 2012; 43: 2132–5. 14. Brown RD, Fleming KD, Meyer FB, Cloft HJ, Pollock BE et al. Natural history, evaluation and management of intracranial vascular malformations. Mayo Clin Proc 2005; 80: 269–81. 15. Beghi E, D’Alessandro R, Beretta S, Consoli D, Crespi V et al. Incidence and predictors of acute symptomatic seizures after stroke. Neurology 2011; 77: 1785–93.
© 2014 The Royal Australian and New Zealand College of Radiologists
R ADIOLO GY—PI CTO R I AL E SSAY
Magnetic resonance imaging in adults with epilepsy: A pictorial essay Jolandi van Heerden,1 Patricia M. Desmond,1 Brian M. Tress,1 Patrick Kwan,2 Terence J. O’Brien2 and Elaine H. Lui1 1 Department of Radiology and 2Departments of Medicine and Neurology, The Royal Melbourne Hospital, The University of Melbourne, Melbourne, Victoria, Australia
J van Heerden MBChB, MMed (radiology), FRANZCR; PM Desmond MSc MDBS FRANZCR; BM Tress MDBS FRANZCR FRCR; P Kwan BMedSci, MBBBC, FRACP, PhD; TJ O’Brien MBBS, FRACP; EH Lui MBBS, MMed (radiology), FRANZCR. Correspondence Dr Jolandi van Heerden, Department of Radiology, The Royal Melbourne Hospital, 300 Grattan Street, Parkville, Melbourne, Vic. 3050, Australia. Email: [email protected]
Summary This pictorial essay highlights the role of the radiologist as a member of the adult epilepsy multidisciplinary team, and gives an overview of MRI-evident epileptogenic lesions. Key words: adult neuroradiology.
neuroimaging;
magnectic
resonance
imaging;
Conflict of interest: None of the authors have conflicts of interest to declare. Disclaimer: No funding was received for this pictorial essay. All the images have been anonymised and were collected retrospectively. Submitted 28 November 2013; accepted 07 December 2013. doi:10.1111/1754-9485.12150
Background Epilepsy is a chronic neurologic condition characterised by recurrent epileptic seizures as clinical manifestations of abnormal, excessive neuronal activity, affecting 0.5–1% of the world population.1 The diagnosis and management of patients with epilepsy have evolved into a multidisciplinary team approach involving neurologists sub-specialised as epileptologists, neurosurgeons, neuropsychiatrists, neuropsychologists, social workers, specialist nurses, counsellors, nuclear medicine physicians and radiologists.1 The primary role of a radiologist is to assess for the presence of structural abnormalities that may be a cause of the epilepsy. Magnetic resonance imaging (MRI) is © 2014 The Royal Australian and New Zealand College of Radiologists
currently the structural imaging modality of choice. Magnetic resonance imaging in combination with clinical assessment, electroencephalography, single-photon emission computed tomography and/or positron emission tomography aid with diagnosis and management. In treatment-refractory cases where multidisciplinary clinical, radiological, nuclear medicine and electrophysiological findings are concordant, surgical resection of a focal epileptogenic lesion situated in a non-eloquent brain region can be considered. In this context, the radiologist can further assist with preoperative planning. Seizure classification is complex and evolving and can be classified by mode of seizure onset (generalised/ focal), aetiology (genetic, structural/metabolic, unknown) or by syndromes.2 Although the precise 1
J van Heerden et al.
terminology is under revision, the clinical importance of whether there is impairment of awareness during a seizure is well recognised. Structural lesions identifiable by MRI often (but not always) present with focal epilepsy and knowledge of typical seizure symptoms and signs can help target the search for a subtle structural lesion (Table 1).1 For instance, focal onset seizures associated with impaired awareness most frequently emanate from the temporal lobe, where the commonest associated structural abnormality is mesial temporal sclerosis (MTS). However, a structural potentially epileptogenic lesion may not be the cause of a patient’s epilepsy, and correlation with clinical, electroencephalography and/or other nuclear medicine imaging findings is essential. Utilisation of a targeted epilepsy protocol will optimise the detection of subtle lesions. Recently, an ‘essential 6’ sequence protocol has been suggested that includes volumetric T1WI, thin-section two-plane fluidattenuated inversion recovery and T2WI (angled to the hippocampi) as well as a haemosiderin/calcificationsensitive sequence.3
a
c
Table 1. Typical seizure symptoms related to various regions of the brain1 Likely location of epileptogenic focus Frontal lobe Mesial temporal lobe
Supplementary motor cortex Motor cortex Sensory cortex
Occipital lobe
Symptoms and signs
Bizarre complex behaviour Forced eye deviation Odd smell Feelings of fear Butterflies in stomach Deja vú Depersonalisation experiences Fencer posturing Focal tonic limb movement Paresthesias Numbness Pain (rare) False sense of inability to move limb Haemianopia Flashing lights Visual distortion Subjective feeling of eye movement Visual hallucination (rare) Nystagmus (rare)
b
d
e
Fig. 1. Mesial temporal sclerosis (MTS). (a) Thin section coronal T2WI MRI showing typical left mesial temporal sclerosis (thick white arrow). The left hippocampus has a reduced volume, loss of internal architectural definition and increased signal. (b) Coronal fluid-attenuated inversion recovery MRI in a different patient demonstrating loss of grey–white matter differentiation in the right anterior temporal lobe with increased signal, often associated with ipsilateral MTS/temporal lobe epilepsy. (c) and (d) Preoperative functional MRI (fMRI) in a patient with left-sided MTS showing ipsilateral language dominance with dominant left Wernicke’s area activation (long white arrow in d) and bilateral Broca’s area activation (short white arrows in c). (e) Post-hippocampectomy sagittal T1WI shows a small volume residual hippocampal posterior body and tail (white arrow).
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© 2014 The Royal Australian and New Zealand College of Radiologists
MRI in adults with epilepsy
Fig. 2. Right amygdala dysplasia. Coronal T2WI MRI shows enlargement with increased signal of the right amygdala (black arrow). Amygdala dysplasia was confirmed histopathologically.
Mesial temporal sclerosis Mesial temporal sclerosis is the commonest epileptogenic abnormality detected on MRI in patients with drugresistant focal epilepsy.4 Well-planned and executed surgical resection in appropriately selected patients with MTS has a good prognosis for long-term seizure control.5 High-resolution coronal T2WI sequences angled to the hippocampi are needed to optimally evaluate for the characteristic changes of MTS, namely increased T2WI signal, reduced volume and loss of architecture in the affected hippocampus (Fig. 1a).4,6 In addition, loss of the
a
b
Fig. 3. Normal variation. Coronal T2WI MRI shows incomplete inversion of the left hippocampus. The left hippocampus is more rounded and vertically orientated with preserved signal. In this case, the internal hippocampal architecture is preserved; however, in some cases, mild blurring may be observed. The adjacent collateral sulcus is vertically orientated (thick white arrow) with resultant irregular shape of the left ventricular temporal horn (black arrow). The left fornix is inferiorly displaced (thin white arrow).
gray–white matter differentiation in the ipsilateral anterior temporal lobe is seen in up to 58% of patients with drug-resistant temporal lobe epilepsy and 64% of patients with MTS (Fig. 1b).7 Less frequently, ipsilateral
c
Fig. 4. Developmental abnormalities. (a) Coronal fluid-attenuated inversion recovery MRI shows type IIb focal cortical dysplasia involving the right superior frontal sulcus with a characteristic ‘transmantle sign’ (thin white arrow) in a patient with other remote left parietal and left temporal regions of trauma-related cortical injury (thick white arrows). (b) Volumetric coronal T1WI MRI shows left parietal polymicrogyria with small irregular gyri and thickened cortex (black arrow). (c) Volumetric axial T1WI MRI demonstrates complex cortical migration and organisation abnormalities with right temporal polymicrogyria (thick black arrow), right temporal closed lip schizencephaly (thin black arrow), as well as abnormal gyration and morphology of the right hippocampus (white arrows). © 2014 The Royal Australian and New Zealand College of Radiologists
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a
Fig. 5. Grey matter heterotopia. (a) Volumetric coronal T1WI MRI shows extensive bi-hemispheric subcortical grey matter band heterotopia (black arrows). (b) Coronal T2WI shows a tiny focus of periventricular nodular grey matter heterotopia along the roof of the right temporal horn (white arrow).
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Fig. 6. Sturge Weber syndrome. (a) Axial contrast-enhanced T1WI MRI demonstrates enhancing left occipital pial angiomatosis (white arrows). (b) Axial T2WI shows left hemispheric atrophy. (c) Susceptibility weighted imaging sequence shows angiomatosis with cortical mineralisation (white arrows). Imaging findings correlated with the clinically evident cutaneous ‘port wine stain’.
a
b
c
Fig. 7. Tuberous Sclerosis. Imaging in a patient with worsening seizures in the context of known tuberous sclerosis previously lost to follow-up demonstrating an interval left frontal high grade glioma. (a) Axial fluid-attenuated inversion recovery MRI shows typical imaging findings related to tuberous sclerosis with left occipital subcortical tubers (short thick black arrow) and right frontal radial glial bands (long thin black arrows) as well as left periventricular sub-ependymal nodules (white arrows). (b) and (c) Coronal contrast-enhanced T1WI MRI and axial MRI cerebral blood volume (CBV) perfusion map demonstrate an interval heterogeneously enhancing left frontal high-grade glial tumour with cortical extension (thick black arrows).
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© 2014 The Royal Australian and New Zealand College of Radiologists
MRI in adults with epilepsy
Fig. 8. Low-grade tumours – histopathologically confirmed. (a) Axial fluid-attenuated inversion recovery MRI shows a non-enhancing low-grade glioma involving the left uncus and amygdala (white arrow). (b) Coronal T2WI MRI demonstrates a dysembioplastic neuroepithelial tumour involving the cornu ammonis (CA1–3) of the right hippocampus (white arrow). (c) Coronal contrast enhanced T1WI shows a ganglioglioma with enhancing (black arrow) and non-enhancing cystlike (white arrow) components involving the left para-hippocampal gyrus and fusiform gyrus.
Fig. 9. Extra-axial tumours causing seizures. (a) Coronal T2WI MRI shows a craniopharyngioma with heterogeneous sellar and supra-sellar proteinaceous cyst-like components impressing on the left mesial temporal lobe (white arrow) that correlated with electroencephalography (EEG) findings. (b) Coronal contrast-enhanced T1WI MRI shows a right fronto-parietal meningioma (white arrow) with adjacent cortical and subcortical signal change (black arrow) with EEG correlation.
Fig. 10. Traumatic brain injury. (a) Axial T2WI MRI shows bi-frontal cortical and subcortical encephalomalacia (white arrows) with ex-vacuo dilatation of the right ventricular frontal horn. (b) MRI susceptibility weighted imaging in the same patient shows trauma-related blood product deposition along the genu and splenium of the corpus callosum (black arrows) as well as bi-frontal cortical superficial siderosis (white arrows).
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© 2014 The Royal Australian and New Zealand College of Radiologists
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fornix and mamillary body atrophy can also be seen.4,6 Bilateral MTS is not uncommon, and there is a known association between MTS and a second epileptogenic lesion, particularly cortical dysgenesis, necessitating careful assessment of the adjacent cortex and amygdala as well as the contralateral hippocampus.4 Altered amygdala signal with volume increase raises the possibility of amygdala dysplasia (Fig. 2) or tumour4 (with post-ictal change a differential), whereas volume loss suggests amygdala sclerosis.6 Preoperative lateralisation of language dominance with functional MRI (Fig. 1c,d) can complement preoperative neuropsychology assessment. A modified partial
a
b
d
e
mesiotemporal resection can be considered in MTS ipsilateral to the side of language dominance to reduce the risk of post-surgical memory-related word-finding difficulty.8 Following hippocampectomy, it is important to comment on the amount of residual hippocampus as well as the extent of post-surgical gliosis to guide decision making if further surgery is considered in the context of seizure recurrence (Fig. 1e). One potential pitfall to be aware of is incomplete hippocampal inversion – a non-epileptogenic congenital variant found in approximately 19% of the general population (Fig. 3).9
c
f
Fig. 11. Infection. (a–c) Axial contrast-enhanced T1WI, diffusion-weighted imaging and apparent diffusion coefficient map show a left occipital rim-enhancing, centrally restricting bacterial abscess (white arrows) with intra-ventricular breakthrough (black arrows). (d) Axial T2WI MRI shows right temporal encephalomalacia as a late consequence of herpes simplex virus encephalitis. (e–f) Axial T2WI MRI and coronal contrast-enhanced T1WI demonstrating the colloidal vesicular stage of neurocysticercosis involving the right anterior temporal pole with marked peri-lesional inflammatory reaction (black arrow in e) and lesional rim enhancement as well as dot-like enhancement of the scolex (white arrow in f).
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© 2014 The Royal Australian and New Zealand College of Radiologists
MRI in adults with epilepsy
with established diagnoses, follow-up imaging should evaluate for interval change (Fig. 7).
Developmental abnormalities Abnormalities of cortical migration and organisation can be subtle and should be carefully searched for using high-resolution volumetric imaging with multi-planar reconstructions. Focal cortical dysplasia (FCD) results from abnormal focal cortical organisation and is categorised into three types on histopathology.10 FCD is classically detected with grey–white matter junction blurring and abnormal subjacent white matter signal.10 Type I is classically associated with focal hypoplasia (‘deep sulcus sign’).10 Type IIb (Taylor’s type with balloon cells) is commonly associated with subcortical white matter hyperintensity tapering towards the ventricle (‘transmantle sign’) (Fig. 4a) best appreciated on T2WI and fluid-attenuated inversion recovery sequences.10 Polymicrogyria and schizencephaly are caused by abnormalities in neuronal migration and cortical organisation and have characteristic radiological appearances (Fig. 4b,c).11 Grey matter heterotopia relates to arrested or disrupted migration of groups of neurons from periventricular germinal zone to cortex and can manifest as periventricular nodular heterotopias, band heterotopias or nodular subcortical heterotopias (Fig. 5).11 In the adult population, the diagnosis of congenital phakomatoses such as tuberous sclerosis and Sturge Weber syndrome (Fig. 6) causing epilepsy is often already established, but occasionally, radiologists may still be the first to suggest these conditions. In patients
a
b
Tumours In young adults with epilepsy, particular tumours to consider include ganglioglioma, dysembryoplastic neuroepithelial tumour (DNET), pleomorphic xanthoastrocytoma (PXA), pilocytic astrocytoma, low-grade glioma and oligodendroglioma (Fig. 8).12 Tumours can have associated FCD (FCD IIIb); thus, peri-tumoural cortex should also be carefully examined.10,11 In the older adult population, high-grade gliomas (Fig. 7b,c), metastases and other rarer tumours that classically involve dural surfaces such as gliosarcomas should be considered.12 Extra-axial tumours can also cause seizures (Fig. 9).12
Trauma Traumatic brain injury resulting in contusions, extraaxial haemorrhages or diffuse axonal injury has a high incidence of both early- and late-onset seizures (Fig. 10).13
Infection Focal seizures can be caused by meningitis but are particularly associated with instances of focal viral or bacterial cerebritis or abscess formation2 (Fig. 11a–d). Atypical organisms such as neurocysticercosis and
c
Fig. 12. Vascular lesions. (a) Axial T2WI MRI shows a right parietal arteriovenous malformation (white arrow) with a superficial nidus involving cortex. (b) Axial T2WI MRI shows the characteristic ‘pop corn’ appearance of two cavernomas involving the right cerebral peduncle (thick white arrow) and right mesial temporal lobe (thin white arrow) with associated circumferential haemosiderin blooming (c) Volumetric axial contrast-enhanced T1WI MRI show developmental venous anomalies (black arrows) associated with the cavernomas shown in (b). © 2014 The Royal Australian and New Zealand College of Radiologists
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tuberculosis can be epileptogenic in all disease phases (Fig. 11e,f).
Vascular Supra-tentorial cerebral vascular malformations most frequently associated with epilepsy are cavernomas and arteriovenous malformations (AVMs), particularly when involving cortex and the temporal lobes (Fig. 12).14 Cavernomas are benign, angiographically occult lesions consisting of intertwined clusters of sinusoidal vascular channels.14 AVMs represent a cluster/nidus of directly communicating arteries and veins without an intervening capillary network.14 Based on size, location and drainage, AVMs are classified using the Spetzler–Martin system for the purposes of surgical prognostication.14 Haemorrhage as a complication in both AVMs and cavernomas can result in seizures even in previously asymptomatic lesions.14 Epileptic seizures can develop as an early or late consequence of both arterial and venous cortical infarcts.15
Conclusion This pictorial essay highlights the radiologist’s role in the adult epilepsy multidisciplinary team and reviews MRIevident epileptogenic lesions that should be considered.
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5. Lowe A, David E, Kilpatrick C, Matkovic Z, Cook M, Kaye A, O’Brien TJ. Epilepsy surgery for pathologically proven hippocampal sclerosis provides long term seizure control and improved quality of life. Epilepsia 2004; 45: 237–42. 6. Chan S, Erickson JK, Yoon SS. Limbic system abnormalities associated with mesial temporal sclerosis: a model of chronic cerebral changes due to seizures. Radiographics 1997; 17: 1095–110. 7. Mitchell LA, Jackson GD, Kalnins RM, Saling MM, Fitt GJ et al. Anterior temporal abnormality in temporal lobe epilepsy: a quantitative MRI and histopathologic study. Neurology 1999; 52: 327–36. 8. Mintzer S, Sperling MR. When should a resection sparing mesial structures be considered for temporal lobe epilepsy? Epilepsy Behav 2008; 13: 7–11. 9. Bajic D, Wang C, Kumlien E, Mattsson P, Lundberg S, Eeg-Olofsson O, Raininko R. Incomplete inversion of the hippocampus – a common developmental anomaly. Eur Radiol 2008; 18: 138–42. 10. Colombo N, Tassi L, Galli C, Citterio A, Russo GL et al. Focal cortical dysplasias: MR Imaging, histopathologic, and clinical correlations in surgically treated patients with epilepsy. AJNR 2003; 24: 724–33. 11. Shorvon SD, Andermann F, Guerrini R (2011) The Causes of Epilepsy: Common and Uncommon Causes in Adults and Children. Cambridge University Press, Cambridge. 12. Beaumont A, Whittle IR. The pathogenesis of tumour associated epilepsy. Acta Neurochir (Wien) 2000; 142: 1–15. 13. Kazemi H, Hashemi-Fesharaki S, Razaghi S, Najafi M, Kolivand PH et al. Intractable epilepsy and craniocerebral trauma: analysis of 163 patients with blunt and penetrating head injuries sustained in war. Injury 2012; 43: 2132–5. 14. Brown RD, Fleming KD, Meyer FB, Cloft HJ, Pollock BE et al. Natural history, evaluation and management of intracranial vascular malformations. Mayo Clin Proc 2005; 80: 269–81. 15. Beghi E, D’Alessandro R, Beretta S, Consoli D, Crespi V et al. Incidence and predictors of acute symptomatic seizures after stroke. Neurology 2011; 77: 1785–93.
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