Focal extratemporal epilepsy: clinical features, EEG patterns, and surgical approach

Journal of the Neurological Sciences 166 (1999) 1–15

Review

Focal extratemporal epilepsy: clinical features, EEG patterns, and surgical approach Roman L. Kutsy* University of Washington /Harborview Medical Center, Box 359722, 325 9 th Ave. NE, Seattle, WA 98104, USA Received 16 April 1999; accepted 19 April 1999

Abstract The objective of this review is a summary of the clinical and electrographic findings in those forms of epilepsy to which the term ‘extratemporal’ (ExT) can be applied. They form a group that differs in many ways from the better known temporal lobe epilepsies. Seizure foci are difficult to localize by clinical semiology alone but modern imaging now often allows a precise definition of the epileptogenic area. The most common causes of ExT epilepsy are tumors and cortical dysgenesis. The concept of ‘dual pathology’ implies the coexistence of two or more distinct lesions, typically mesial temporal sclerosis and cortical dysplasia. Electroencephalography (EEG) and electrocorticography (ECoG) are valuable tests in the definition of the epileptogenic area beyond the structural lesion, and surgical removal must be guided by the nature of the lesion and the extent of the epileptogenic zone.  1999 Elsevier Science B.V. All rights reserved. Keywords: Extratemporal epilepsy; Temporal lobe epilepsy; EEG; Electrocorticography; Cortical dysgenesis; Dual pathology; Surgical outcome; Review

1. Introduction Electroencephalography (EEG), neuroimaging, and longterm monitoring have aided in the characterization of many types of focal epilepsy. ‘Typical’ temporal lobe seizures originating in the hippocampi the parahippocampal gyri, and the amygdaloid nuclei constitute the majority of focal epilepsies and gain the most benefit from surgery [36]. In contrast, extratemporal (ExT) epilepsy constitutes a more heterogeneous group. Different types of focal ExT epilepsies manifest themselves by a wide range of epileptic seizures and show highly variable responses to therapy. Extratemporal epilepsy can be classified according to the *Tel.: 11-206-731-3502; fax: 11-206-731-8545. E-mail address: [email protected] (R.L. Kutsy)

presumed site of seizure origin. Frontal, parietal, and occipital focal epilepsies exist, and multiple territorial overlaps may occur [96,98]. The ExT epilepsies are common disorders. According to the National General Practice Study of Epilepsy [75] at the Chalfont Centre for Epilepsy in England, 26.9% of all patients with definite epilepsy had seizures of identifiable focal origin. Within this group 22.5% had frontal, 32.5% central, 5.6% frontotemporal, and 6.3% each parietal and occipital foci, with only 27% of the patients having temporal lobe abnormalities. A larger more recent study [109] at the Epilepsy ˆ ` Hospital in Paris included 1369 Unit of the La Salpetriere patients with partial epilepsy of whom 814 had identifiable lesions by magnetic resonance imaging (MRI). One hundred and seventy-nine (22%) had frontal, 20 (2.5%) occipital, and 15 (2%) parietal epilepsies. It is not always

0022-510X / 99 / $ – see front matter  1999 Elsevier Science B.V. All rights reserved. PII: S0022-510X( 99 )00107-0

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clear how the type of epilepsy affects the outcome of medical or surgical therapy. This retrospective review attempts a correlation of clinical findings, EEG and electrocorticography (ECoG), and surgical success rates, and the goal is to guide the neurologist toward the most rational management in their patients with ExT epilepsy.

2. Clinical features The manifestations of ExT epilepsy are variable, and localization by clinical signs alone remains difficult. A few types of ExT seizures are stereotypical and characteristic of certain epileptogenic sites. Generally, ictal semiology is diagnostic when seizures arise from a primary cortical area, such as the primary motor, visual, or sensory cortices.

2.1. Localizing extratemporal seizures 2.1.1. Focal clonic motor seizures Also known as ‘Jacksonian’, these simple partial motor seizures originate in the primary motor (Rolandic) cortex (area 4). Typically, consciousness remains intact, and secondary generalization occurs rarely. Jackson [54] described three variants of these seizures: (1) ‘fits starting in the hand (most often in the thumb or index-finger, or both)’; (2) ‘fits starting in one side of the face (most often near the mouth)’; and (3) ‘fits starting in the foot (nearly always in the great toe)’. 2.1.2. Supplementary motor area ( SMA) seizures First described more than 50 years ago by Penfield and Erickson [93], these seizures represent a unique constellation of very complex and stereotypic features. Classic signs of SMA seizures include sudden abduction of the contralateral arm with flexion at the elbow and forced contralateral deviation of the head followed by forced vocalization, shriek, or speech arrest [94,97]. Clonic activity in the contralateral face, arm, or secondary generalization occurs frequently. Versive head deviation is strongly associated with frontal seizure onset only when it occurs early in the seizure [24,74]. Speech arrest occurs only when the seizure focus involves the superior frontal gyrus on the dominant side. These seizures are characteristic of partial epilepsy of dorsolateral frontal origin (area 6) and are highly reproducible by the direct cortical stimulation of this particular area [1]. However, such seizures may also be seen with parasagittal frontal [97], frontopolar or orbitofrontal [74], or occasionally extrafrontal (parietal or occipital) epilepsy [129,132]. 2.1.3. Occipital lobe phenomena Certain signs are characteristic of a seizure origin in the occipital lobe. Simple visual hallucinations and acute blindness are the most typical, and sometimes sole [110], occipital lobe seizure phenomena [5,10,104,132]. Visual

hallucinations present as flashing or steady, colored or achromatic simple geometric figures that may occupy half of the visual field contralateral to the seizure origin. Other features suggesting an occipital seizure origin, such as forced eye blinking, may occur with seizures originating elsewhere [130,132].

2.1.4. Parietal lobe phenomena Somatosensory disturbances as part of an aura occur in 63% of seizures of parietal origin [105]. Tingling and numbness contralateral to the epileptogenic parietal lobe are the most common symptoms though bilateral sensory disturbances may also occur [1,114]. Sixteen percent of such patients may experience contralateral body pain. Another common parietal phenomenon is disturbance of body image. It occurs in 11% of the patients with parietal epilepsy and typically presents with a sensation of movement in one extremity or a feeling that an extremity is absent [105]. Though these symptoms are considered characteristic parietal lobe phenomena, they may also be provoked by direct cortical stimulation of both post- and precentral regions [39,92]. 2.2. Poorly localizing extratemporal seizures 2.2.1. Complex partial and secondarily generalized seizures Many clinical features allow the distinction between temporal and ExT seizures. However, difficulties arise when the epileptogenic zone is unusually large and poorly defined [97,98]. Complex partial seizures (CPSs) were divided into two types by Delgado-Escueta and co-workers [28,29,126]. Type I included ‘typical’ temporal lobe seizures with motionless stare, quasi-purposeful movements, and orofacial automatisms, while type II seizures showed postural or focal movements, automatic ambulation, and agitation. Type II seizures were suggestive of ExT epilepsy and were not benefited by temporal lobectomy [126]. Subsequently, Brey and Laxer [12] reported that type I and type II seizures may coexist. Many reports supported the idea that CPSs could be differentiated into temporal or ExT types based on clinical information [128,130,131]. Other studies showed no specific differences in seizure types [118]. Manford et al. [74] analyzed 352 seizures in 252 patients and established that relatively few could be localized reliably on clinical grounds. Frontal lobe epilepsy is the most common in the ExT group. In a recent study comparing the accuracy of ictal semiology of frontal and temporal seizures, only 61% of frontal lobe seizures were localized correctly. Twenty percent of frontal lobe seizures caused symptoms suggestive of temporal lobe epilepsy [84]. Table 1 compares the clinical features of CPSs of frontal and temporal origin [6,24,25,40,41,73,74,78,80,81,97,106,122,130,131,135]. Rarely, seizures may emanate from the sensorimotor

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Table 1 A comparison of clinical features of frontal and temporal epilepsies

Duration of seizures Onset and offset Aura of fear Epigastric aura ´ ` vu and jamais vu Aura of deja Aura of olfactory hallucinations Unilateral dystonic limb posturing Tonic posturing Contralateral head and eye turning (version) Ipsilateral head and eye turning Autonomic signs Vocalization Visual and auditory hallucinations ‘Forced’ thinking Oroalimentary automatisms Gestural automatisms Sexual automatisms Motor agitation and bizarre behavior Bilateral clonic activity with preservation of consciousness Ictal bradycardia Painful auras and ictal pain The time of progression from initial non-motor phase to clonic activity a Predominant occurrence at night History of febrile seizures c History of status epilepticus Clusters of seizures Postictal changes

Frontal epilepsy

Temporal epilepsy

Brief Sudden Unusual, may be seen with frontal medial onset Very unusual Very unusual Unusual, may be seen with orbitofrontal onset Unusual

Usually longer Less precipitous Very common

Common Common, particularly with SMA seizures May be seen with anterofrontal seizures Unusual, may be seen with orbitofrontal and insular onset Common Unusual, may be seen with orbitofrontal and SMA onset Unusual, may be seen with dorsolateral SMA onset Unusual Unusual May be seen Common

Very common Common Very common Very common lateralizing sign Common Much less common Unusual Common Unusual Common More common Very common Very common Unusual Unusual

May be seen

Not seen

Not seen May be seen Short (mean 2 s)

May be present Unusual Long (mean 47 s)

Common Rare (5.6%) More likely Common Minimal

Rare b Common (25.2%) Less likely Rare Prominent

a

As reported by O’Brien et al. [84]. Features of nocturnal temporal lobe epilepsy were described by Bernasconi et al. [9]. c Based on a review 133 patients with febrile seizures among 1005 epileptics [49]. b

face area. They may present initially with speech arrest, tongue movement, or focal clonic activity of the face as part of a highly localizing ‘Jacksonian’ pattern. With progression of the seizure, they usually evolve into tonic or atonic drop attacks [66,88] or ‘typical’ temporal lobe seizures due to spread to the mesial temporal structures [66]. Other ExT epilepsies, including parietal and occipital, demonstrate even greater variability of symptoms depending largely on the route of seizure spread [114]. Williamson et al. [132] commented on two preferential modes of occipital seizure spread influencing the main clinical manifestations: propagation into the medial temporal structures resulting in ‘typical’ temporal lobe seizures, and spread via a more superior pathway into the frontal lobe leading to a ‘frontal’ seizure type. In a group of 35 patients

with lesional occipital lobe epilepsy, 11 had temporal lobe seizure type, eight had a frontal lobe seizure type, and 10 demonstrated more than one type of seizure. In addition, secondary generalization was present in 24 patients [5]. Salanova et al. [105] studied 82 patients with parietal lobe epilepsy and showed that 61% of the patients with the tonic posture of frontal lobe epilepsy actually had epileptogenic zones in the superior parietal lobule. Seventynine percent of patients with automatisms resembling temporal lobe seizures had epileptogenic zones in the inferior parietal lobule. This observation reflects the preferential seizure spread from the parietal lobe to adjacent areas [105,129].

2.2.2. Pseudoabsences and myoclonus These seizures can masquerade as ‘typical’ absences of

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primary generalized epilepsies presenting with speech and behavioral arrest, eye opening, alteration of consciousness, occasional simple automatisms, and quick recovery. They were first described in patients with parasagittal frontal ¨ lesions by Tukel and Jasper [120]. Pseudoabsences are also seen with seizures of frontopolar origin [6]. Manford et al. [74] found pseudoabsences to be more common among patients with temporal lobe epilepsy. In their group, patients with frontal lobe epilepsy and absence seizures had lesions in the mesial frontal and, less frequently, orbitofrontal regions. Several patients with clinical and EEG features of absence status emanating from the frontal lobe were also described [59]. Myoclonus can be a rare manifestation of focal epilepsy originating in the primary motor area. It is usually associated with focal motor seizures and may be caused by tumor or rolandic cortical dysplasia [62].

3. EEG findings

3.1. Interictal EEG abnormalities Several types of interictal patterns may be seen in patients with ExT epilepsy. They include: (1) focal interictal epileptiform discharges (IEDs) localized to the site of seizure origin; (2) regional, poorly localized, but lateralized IEDs; (3) falsely localizing focal IEDs; (4) multifocal IEDs; (5) bilateral or generalized, bilaterally synchronous IEDs; and (6) no IEDs. Different degrees of focal or diffuse non-epileptiform electrographic changes may also be present.

3.1.1. Focal IEDs localized to the site of seizure origin Focal IED are often absent in ExT epilepsy. When present, they may refer to different regions of the frontal, parietal, and occipital lobes. Fig. 1A–E represent examples of focal IEDs of different location. Quesney et al. [98] analyzed the distribution of IEDs among 34 patients who became seizure-free after surgery on the frontal lobe and found that only three patients (9%) had preoperative focal spikes. When patient selection is limited to cases of lesional epilepsies, the proportion of focal IEDs increases [74]. However, even in this group of patients, focal localizable IEDs are seen in less than half of all cases and tend to correlate with certain type of seizures, particularly version SMA type and seizures with ‘bizarre’ motor agitation. The most recent study of EEG features of frontal lobe epilepsies also concluded that patients with seizures originating in the dorsolateral frontal area tend to have focal IEDs [8]. Of the 35 patients with occipital epilepsy studied by Aykut-Bingol et al. [5], only six (17%) demonstrated interictal discharges that were localized to the occipital region. Similar frequency of focal IEDs is observed among patients with parietal epilepsy. Salanova

et al. [105] encountered focal parietal discharges in six out of 66 patients (9%). A preponderance of focal localized IEDs may also reflect the underlying pathology. In occipital lobe epilepsy caused by malformations, the incidence of focal occipital IEDs (29%) was much higher than in seizures caused by tumors [5]. Raymond et al. [100] observed focal IEDs in 47% of their patients with different types of cerebral cortical dysgenesis, bilateral IEDs in 13%, focal and bilateral IEDs in 25%, and absent IEDs in 15%. Another interictal EEG feature of underlying cortical dysplasia is rhythmic epileptiform discharge. Forty-four percent of patients with developmental abnormalities of the cortex showed this pattern [42,90]. In 60% of these patients, rhythmic epileptiform discharge presented as trains of repetitive 4–10-Hz spikes with a duration of 1–4 s. In another 40%, it was seen as continuous 2–7-Hz sharp waves [42].

3.1.2. Regional, poorly localized, but lateralized IEDs When present, this type of interictal epileptiform abnormality is useful in the lateralization of the possible epileptogenic zone. It alerts the clinician to the possible presence of ExT rather than temporal lobe epilepsy. Regional, poorly localized IEDs may be seen over broad hemispheric regions (Fig. 1F). In a group of patients with frontal lobe epilepsy, Quesney et al. found regional spiking in 59% [98]. In patients with occipital and parietal epilepsies, regional IEDs were observed in 24% [5] and 60.5% [105], respectively. 3.1.3. Falsely localizing and multifocal IEDs Focal IEDs that are completely discordant with the site of seizure origin may be misleading (Fig. 1G). They may be present in ExT epilepsies of any lobar location, but most commonly in occipital epilepsy. Up to 27% of patients with occipital lobe epilepsy have focal temporal IEDs [5]. Patients with an epileptogenic zone in the frontal insular-opercular and orbitofrontal regions also tend to have a high incidence of falsely localizing temporal IEDs. [80]. Moreover, up to 90% of patients with temporal lobe epilepsy may show a spread of IEDs from the anterior temporal to fronto-polar regions. The latter pattern was postulated to be due to inherent physiological properties of fronto-temporal circuits [35]. Multifocal IEDs, although considered to be a sign of severe ‘non-surgical’ epilepsy and mental retardation [82], may be seen in focal epilepsies of ExT origin, particularly in medial frontal epilepsy [8] and in certain brain malformations such as the congenital bilateral perisylvian syndrome [61] (Fig. 1H). 3.1.4. Bilateral or generalized, bilaterally synchronous IEDs ¨ Tukel and Jasper described a phenomenon of secondary bilateral synchrony in 1952 [120]. Initially, it was considered to be limited to parasagittal or inferior frontal

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Fig. 1. Different types of epileptiform discharges. Digital EEGs were recorded and displayed in referential montage (average reference). Electrodes are labeled according to the 10–20 system. (A) Left frontopolar IEDs in a 34-year-old man with nocturnal generalized tonic–clonic seizures and cortical dysplasia in the left orbitofrontal region. Subsequent intracranial EEG monitoring was concordant with MRI findings. (B) Left midfrontal multiple spikes in a 23-year-old woman with CPSs and normal MRI. Invasive intracranial EEG monitoring demonstrated a focal seizure onset in the left superior frontal region. (C) Right central spike in a 32-year-old woman with frequent focal motor ‘Jacksonian’ seizures and a low-grade glioma in the right Rolandic area. (D) Left parietal sharp wave in a 42-year-old man with simple sensorimotor and complex partial seizures with occasional secondary generalization caused by the left parafalcine meningioma. (E) Very brief left occipital spike in a 38-year-old woman with epilepsy as a result of CNS vasculitis complicated by an occipital infarct. (F) Poorly localized, predominantly left hemispheric spike-and-wave discharge in an 18-year-old man with frequent partial and secondarily generalized seizures and large left frontal cerebral malformation. (G) Falsely-localized; left basal temporal IED in a 34-year-old man with nocturnal generalized tonic–clonic seizures and cortical dysplasia in the left orbitofrontal region. (H) Multifocal IEDs (bilateral basal temporal and left mid-posterior temporal) in a 20-year-old man with severe epilepsy, mental retardation, and left parietal porencephaly. (I) Secondary bilateral synchrony. This burst of generalized three-per-second sharp-and-slow waves followed by more focal left frontal spikes was seen in a 19-year-old man with daily simple partial motor and complex partial seizures and normal MRI. Invasive intracranial EEG monitoring demonstrated a focal seizure onset in the left primary motor hand and face area.

epileptogenic lesions; however, it was also described with posterior hemispheric lesions [21] and in up to 32% of patients with parietal lobe epilepsy [105]. Blume and Pillay [11] reported this phenomenon in 0.5% of more than 10 000 consecutive EEGs. In more than half of these patients, secondary synchrony originated in the frontal (primarily superior frontal) region, however, 96% of their patients had more than one and 77% had multifocal independent interictal foci. Fig. 1I, depicts a phenomenon of secondary bilateral synchrony. Clinical correlates of secondary bilateral synchrony are atypical absences, myoclonic jerks, different types of CPSs, or tonic / atonic seizures. Among 31 patients with ‘drop attacks’ in recent series of Tinuper et al. [119], 74% showed secondary bilateral synchrony on EEG and 71% had frontal lobe epilepsy. Secondarily generalized and bisynchronous IEDs usually demonstrate very small interhemispheric time

difference. When measured using Gotman’s method of interchannel coherence during fast Fourier transform (FFT) analysis, interhemispheric time difference averages 15 ms [44]. Another study estimating interhemispheric time difference by FFT analysis concluded that a difference of more than 9.3 ms is suggestive of secondary bilateral synchrony, while a difference of less than 5.8 ms is compatible with the diagnosis of primary generalized epilepsy [58]. Secondary bilateral synchrony may be disrupted during Wada testing [71] or after anterior callosotomy [85]. These tests may be useful as intermediate steps to localize ‘difficult’ epileptic foci that are obscured by secondary bilateral synchrony.

3.1.5. Absent IEDs Quesney cited ‘absence or paucity of IEDs’ as one of the features of ExT epilepsy [96]. It is contrasted by a

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Fig. 1. (continued)

R.L. Kutsy / Journal of the Neurological Sciences 166 (1999) 1 – 15

much more universal presence of IEDs in temporal lobe epilepsy. Certain locations and seizure types are less accessible to the standard scalp EEG, e.g. three of five patients with medial frontal lobe epilepsy in one series [8] and 11 of 14 patients with ‘Jacksonian’ motor seizures in another [74].

3.2. Ictal EEG abnormalities 3.2.1. Scalp EEG Localization of the seizure origin in ExT epilepsies may be hindered by many factors. The most important is a large size of the epileptogenic zone [1,37,96,98,107]. Quesney et al. [98] observed ‘focal accentuation’ in 23.3%, ‘regional configuration’ in 50%, and ‘multilobar distribution’ in 16.7% of his cases. In parietal epilepsy, widely distributed lateralized but poorly localized ictal patterns are seen in up to 90% of all seizures [105]. In occipital epilepsy, nearly 50% of patients with cortical dysplasia had localized occipital discharges, while patients with occipital lobe tumors almost never exhibited localized ictal patterns [5]. In a recent study of 86 patients with neocortical epilepsy, Lee and Kim [64] found discrete ictal EEG changes in 23% of patients with frontal, 70% with occipital, and 10% with parietal epilepsies. Absence of ictal EEG changes is another problem in the localization of ExT [96]. Medial frontal [8] and ‘jacksonian’ motor [74] seizures are among the commonest in this group. Several unique electrographic ictal patterns occur in ExT, particularly in frontal epilepsies. Secondary bilateral synchrony has already been discussed. A diffuse ‘electrodecremental’ ictal pattern may offer a hint of focal frontal seizure onset despite its apparently generalized appearance. In a group of 39 patients with diffuse electrodecremental responses, Arroyo et al. [3] found that 23 patients had ictal behavior suggestive of a frontal seizure origin and seven patients revealed mesiofrontal seizure onset (recorded by intracranial monitoring). Focal rhythmic fast activity is seen much more commonly with ExT rather than temporal epilepsies. Bautista et al. found this pattern to be characteristic of frontal seizures of dorsolateral origin [8]. Electroencephalographers should be aware of the misleading, seemingly frontal ictal activity in temporal lobe epilepsy. Named ‘frontopolar ictal epileptiform discharge’ by Mikuni et al. [76], this particular pattern manifests with rhythmic, unilateral predominantly frontopolar ictal activity in the d –u range. It is seen among patients with temporal lobe epilepsy and may be explained by dipolar orientation of ictal activity that originates in the lateral rather than the basal temporal region. Despite the difficulties listed above, lateralization of the ExT seizures is possible in 47–65% (comparing with 76–83% for temporal seizures) [125]. Localization, how-

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ever, usually requires some type of invasive monitoring, particularly when no structural pathology is present on neuroimaging studies.

3.2.2. Electrocorticography ( ECoG) Long-term extraoperative invasive EEG monitoring with intracranial grid and strips electrodes is the ultimate step in establishing the location of seizure origin. Problems with recording from implanted electrodes include a large size of the epileptogenic zone [1,37,96,98,107], sampling error [130], rapid propagation of the seizure, and occasional epileptic progression along different pathways in the same patient [96,129,130]. Kutsy et al. [60] monitored 26 patients with neocortical epilepsy with intracranial electrodes and found 46% with large epileptic zones, 23% with small focal epileptogenic zones, and 31% with multifocal seizure onset. Fifty percent of their patients revealed rapid contiguous spread of ictal patterns (less than 1 s), 31% slow contiguous spread, and 19% distant non-contiguous spread. Despite difficulty in localization of the epileptogenic zone, intracranial EEG monitoring may be used successfully even in the most challenging cases. Some of the cortical lesions demonstrate unique ECoG patterns. For instance, areas of cortical dysplasia may generate continuous epileptiform discharges recorded during ECoG in up to 67% of these patients [42]. Electrocorticography is useful in the assessment of postictal changes [52]. Postictal slow foci were present in one-third of patients with ExT epilepsy compared with two-thirds of patients with temporal lobe seizures. These changes usually occurred when a seizure lasted longer than 32 s, and this observation may offer an additional clue for the localization of the epileptogenic zone.

4. Causes of extratemporal epilepsy Jackson [55] recognized that structural brain pathology, such as a tumor, may cause epilepsy. With progress in neuroimaging, the proportion of ExT epilepsy cases without an identifiable focal brain lesion decreased significantly and now constitutes probably 20–40% of all ExT epilepsy cases [34,83]. Table 2 presents the rate of occurrence of different radiological and histopathological findings in ExT epilepsies. Brain tumors and developmental cortical disorders are the two largest etiological groups that are responsible for 30–70% of all ExT epilepsies [91]. Coexistence of two or more different types of epileptogenic lesions, otherwise known as ‘dual pathology’, is another common type of abnormality. Epilepsy may also be the only symptom of either a primary brain tumor [79] or a congenital cerebral malformation [100], necessitating neuroimaging in every new case of focal epilepsy.

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Table 2 Histopathological and radiological findings in extratemporal epilepsies

Neoplasms (%) Developmental malformations (%) Trauma (%) Vascular malformations, strokes and anoxic injuries (%) Rasmussen encephalitis (%) Infectious encephalitis or meningitis (%) Abscess (%) Non-infectious inflammation (%) Lafora body disease (%) Arachnoid cyst (%) Non-specific gliosis or ossification (%) No structural abnormalities (%) a b

Talairach et al. [116] n5100

Wolf et al. [133] n563

Vital et al. [123] n585 a

Zentner et al. [137] n560

Aykut-Bingol et al. [5] n535 b

Kutsy et al. [60] n526

Kim et al. [57] n524

15

19 25.4

17 25

28 15

37 40

11.5 23

16 68

15 18

11.1 11.1

20

16.5

3

15 15

4.7 15

1.7

11.5

1.7

1.5 16.5

4 3

8 4

37

11.1

13

22

14

14.3

16.5

17

3

4

16

12

Includes cases with ‘dual pathology’. Includes cases of occipital lobe epilepsy only.

4.1. Congenital cortical dysgenesis Cortical dysplasia is the commonest type of focal congenital cortical dysgenesis. Cortical dysplasia as a cause of epilepsy was first described by Taylor et al. [117]. In the beginning, it was considered an uncommon disorder [108]. However, with the advent of neuroimaging, many cases of previously considered ‘idiopathic’ epilepsies evolved into multiple groups [109]. Many patients with cortical dysplasias and epilepsy underwent surgical resections of their lesions [87–89,95,100]. Mischel et al. [77] made a systematic analysis of the pathology of cortical dysplasia. They found laminar disorganization, single heterotopic white matter neurons and frank heterotopias, abnormal neurons in the molecular layer, a persistent subpial granular layer, marginal glioneuronal heterotopia, micropolygyria, neuronal cytomegaly with abnormal cytoskeletons, and ‘balloon’ cell change. Many additional features of cortical dysgenesis associated with ExT epilepsy have been described in recent years. They include congenital bilateral perisylvian syndrome [61], periventricular and subcortical nodular heterotopia [32], X-linked bilateral periventricular nodular heterotopia [53,102], X-linked bilateral periventricular nodular heterotopia associated with frontonasal malforma-

tion [46] and syndactyly [30], ‘double cortex’ syndrome [86], and sublobar dysplasia [7]. Other types of congenital cerebral dysgenesis with epilepsy and survival into the adulthood include agyria, macrogyria, and cortical ‘tubers’ of tuberous sclerosis complex. Certain brain tumors may be classified with cortical dysgenesis rather than neoplasms. They include hamartomas [124] and dysembrioplastic neuroepithelial tumors [27]. Though the latter may show mitoses, cell proliferation is generally very slow [100]. Raymond et al. [100] studied 100 patients with different types of cortical dysgenesis. Their diseases included generalized (16%) and localized (84%) epilepsy of frontal (38%), temporal (37%), parietal (17%), and occipital (8%) origins. Ten patients had developmental delay and 15% revealed focal neurological deficits. In 18 of 84 patients with focal epilepsy in this group, ictal electrographic patterns were discordant with the site of cortical dysgenesis. This discrepancy may be due to the multiplicity of dysgenesis. Sisodiya et al. [111] reported that 15 of 18 patients with cortical dysgeneses had electrographic abnormalities beyond the margins of the lesion visualized by volumetric MRI. Nine of 10 patients with unilateral lesions had abnormalities in the contralateral hemisphere when quantitative MRI techniques were used. Some pa-

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Table 3 Incidence of dual pathology among patients with MRI-confirmed medial temporal sclerosis Levesque et al. [67] Number of patients Patients with dual pathology (% of total) Patients with dual pathology who have cortical dysgenesis (%) Patients with dual pathology who have porencephaly (%) Patients with dual pathology who have neoplasms (%)

Cendes et al. [20]

178 68 54 (30.3%) 8 (14%)

13 (24%)

Not specified 12 (22.2%)

5 (62.5%)

Raymond et al. [101] a

Li et al. [69] b

100 15 (15%)

254 167 24 (9.5%) 25 (15%)

15 (100%)

0

0

2 (25%)

0

14 (58%)

Not specified 7 (29%)

Cendes et al. [19]

12 (48%)

Pasquuier et al. [91]

Li et al. [68]

195 14 (7.2%)

64 14 27 13 (20.3%) 13 (93%) 14 (52%)

6 (43%)

7 (54%)

5 (20%)

0

0

1 (4%)

5 (36%)

1 (7.7%)

Ho et al. [51] c

0

Sisodiya et al. [112]

14 (100%)

–d 13 (100%) 0

0

0

Semah et al. [109] 1148 44 (4%)

Notspecified Notspecified Notspecified

a

All patients in this study had cortical dysgenesis. Not every patient in this study had medial temporal sclerosis. Only 17 patients had hippocampal atrophy as part of dual pathology. The remaining seven patients had a combination of other pathologies. c This study only included patients with congenital porencephaly. d All 14 patients had cortical dysplasias evident by volumetric MRI studies only. Two patients in this group also had ‘visible’ subependymal heterotopias. b

tients with cortical dysgenesis had different types of cerebral structural abnormalities, a phenomenon known as ‘dual pathology’.

4.2. Dual pathology The term ‘dual pathology’ was proposed by Levesque et al. [67] to emphasize the clinical importance of the coincidence of ExT lesions with medial temporal sclerosis. Several authors reported the coincidence of hippocampal abnormalities and neocortical lesions (see Table 3). The highest comorbidity was found between medial temporal sclerosis and cortical dysgenesis [100], porencephalic cysts [19,51,100], and periventricular heterotopia [101]. Coexistence of lesions other than medial temporal sclerosis may also occur, e.g. cortical dysgenesis and neoplasms [100] or neoplasms and vascular malformations [69]. Seizures due to dual pathology are often refractory to medical management. Only 3% of non-surgical patients with dual pathology were seizure-free in long-term follow-up in the series reported by Semah et al. [109]. The presence of dual pathology should prompt a surgical approach to remove both the neocortical epileptogenic lesion and the sclerotic hippocampus [15,68].

5. Surgical outcome Long-term outcome after surgery for ExT seizures depends on many factors. Generally, the benefit of surgical treatment for ExT epilepsy is less impressive than operations for medial temporal epilepsy. However, recent

studies in pediatric epilepsy did not find a statistical difference between the outcomes after surgical treatment of temporal and ExT epilepsy [33,134]. Seizure-free outcome rates were 10% for selected temporo-parietal and occipital cases [38], 26% in a large retrospective review of Montreal Neurological Institute [99], 43% in a multicenter study [36], and 53.7% in a retrospective review at the Institute of Neurosurgery, Rome, Italy [103]. The factors that influence long-term postoperative outcome can be divided into several groups.

5.1. The presence of a structural lesion The presence of a structural lesion is the single most important criterion in predicting surgical outcome. Talairach et al. [116] reported surgical success in 35 of 46 patients (76%) with localized frontal lesions and in 11 of 18 patients (61%) without structural abnormalities. Van Ness [121] discussed several factors relevant to postoperative seizure relief and came to the conclusion that the presence of a lesion on a neuroimaging study correlates with better outcome. The absence of a lesion or imaging abnormality was an unfavorable prognostic sign [137]. However, some reports claimed that the presence of a structural lesion was not significantly associated with outcome [103]. Rather, structural lesions were thought to be predictors of higher interictal electrograhic abnormalities that in turn influenced the postoperative prognosis [103]. Lorenzo et al. [72] studied 48 patients with intractable frontal lobe epilepsy and observed that patients without MRI abnormalities did better than those with multilobar structural lesions.

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5.2. The nature of the structural abnormality The nature of the epileptogenic lesion may significantly influence surgical outcome despite similar operative technique and degree of excision. Although the presence of an identifiable structural lesion is a favorable prognostic feature, not all types of lesions convey the assurance of postoperative freedom from seizures. Cortical dysgenesis has been associated with the worst surgical outcomes [50]. The reason may be the multiplicity of lesions, structural abnormalities that are not apparent on neuroimaging studies, and poor congruence of electrographic and radiological findings. Epileptogenic zones in cortical dysgenesis are usually more extensive than the visible lesion and are multilobar in more than 70% of patients [87,88]. Other features that correlate with a worse surgical outcome in cortical dysgenesis are lesions outside the temporal and frontal lobes and generalized IEDs [50]. Only two of 24 patients in the series reported by Palmini et al. [87] became seizure-free. Eight achieved a 90% reduction in seizure frequency. An overall favorable outcome was achieved in 42% of the patients. Six of 17 patients (35%) reported by Hirabayashi et al. [50] and eight of 25 (32%) described by Kim et al. [57] became seizure-free. Taylor et al. [117] reported better outcomes in the original study of cortical dysplasia, where six out of 10 patients (60%) became seizure-free postoperatively. Excellent surgical outcomes were reported for patients with hamartomas (77% seizure-free) [124]. Smith et al. [113] reported significantly better outcome in patients who were younger than 18 years. However, Wyllie et al. [134] reported that long-term outcome in 136 children with ExT epilepsy due to cortical dysplasia was less favorable when compared to other lesions. When patients with tuberous sclerosis have only one tuber, the postoperative prognosis is favorable. In study of 12 patients undergoing cortical resection for tuberous sclerosis, 58% became seizure-free [45]. Others reported similar outcomes for epilepsy surgery in tuberous sclerosis [4]. Surgical outcomes are generally favorable in patients with tumors. Zentner et al. [137] studied 60 patients with ExT epilepsy. Eighty percent of those with tumors (15 patients) became seizure-free. In contrast, only 52% of patients with non-neoplastic lesions became seizure-free. Goldring et al. [43] also demonstrated an 82% seizure-free rate among their patients with gliomas. Another study of 51 patients with low-grade glial tumors provided almost identical outcome figures, 66% seizure-free and 88% significantly improved [13]. Laoprasert et al. [63] reported an 89% seizure-free outcome for patients with complete tumor resection and 63% for those with partial resection. When only patients with tumors and cortical dysgenesis of the occipital lobe were compared, a significant difference in outcome was found as well [5]. In the tumor group, 84.5% improved, while in the dysplasia group, only 45% had good outcomes.

Arteriovenous malformations may also correlate with better surgical outcome [31]. Yeh et al. [136] showed that a better outcome is expected among patients whose age at seizure onset was greater than 30 years and who had an epilepsy duration of less than 1 year. Cavernous malformations are also associated with excellent outcome, particularly if patients had less than five seizures prior to surgery and less than a 12-month history of epilepsy [14]. More restricted prognostic criteria for curative cavernous malformations surgery were suggested by Cohen et al. [23] who described 100% seizure-free outcomes in patients with single preoperative seizures or a history of epilepsy of less than 2 months. In contrast, only 50–55% of patients with more than five preoperative seizures and more than 12-month history of epilepsy became seizure-free [23]. Epilepsy resulting from head injury generally shows an unfavorable outcome because lesions tend to be multiple. Nevertheless, several authors reported excellent surgical outcomes (70–100% seizure-free) [26,56]. A past history of CNS infection usually implies a very poor postoperative prognosis [65].

5.3. Location of the lesion and epileptogenic zone Surgical outcomes for frontal, parietal, and occipital lobe epilepsies are comparable [5,105,116] but some authors believe that ‘pure’ frontal lobe epilepsies benefit more from surgery than other forms. Swartz et al. [115] studied 37 patients with frontal lobe epilepsy and determined that 19 had a focus confined to the frontal lobe, while 12 had additional extrafrontal foci. Sixty percent of the ‘pure-frontal’ group became seizure-free, while only 10% of the extrafrontal group had similarly favorable outcomes. Differences in surgical outcome persist when variable areas within the anatomical brain regions are assessed. Rasmussen [99] reported that 47% of patients with anterior and 35% of patients with lateral frontal resections became seizure-free, compared to only 18% of patients with parasagittal resections and 10% of patients with extension of the excision into parietal and temporal lobes. In contrast, Talairach et al. [116] reported the best outcomes for patients with fronto-temporal and posterior medial frontal resection (80% of patients had more than 75% reduction in seizure frequency), followed by central (60%), anterior medial frontal (50%), and prefrontal (45%) groups. In occipital lobe epilepsies, patients with medial or lateral occipital resections do not differ significantly in outcome [5].

5.4. The approach to cortical resections Two main surgical approaches exist for patients with structural lesions: excision of the lesion (lesionectomy) without prior long-term intracranial monitoring or intraoperative ECoG; and cortical resection based on combined radiological and electrophysiological data. Lesionectomy

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has been the most valuable approach for patients with cerebral neoplasms [43,63]. Stereotactic lesionectomy may be an effective mode of surgery for all types of lesional epilepsies [2,16,31]. Cascino et al. [17] found that 74% of patients had more than 90% reduction in seizure frequency after stereotactic lesionectomy. Fifty-six percent became seizure-free. Other authors [70] suggested that lesionectomy may be a first-step procedure for ExT epilepsy due to low-grade gliomas if EEG concordance is present. Lesionectomy is the procedure of choice for patients with cavernous malformations who had seizures for less than 2 months and only one attack before the operation. Cortical resection may be reserved for those with a longer history of epilepsy related to the malformation [23]. Patients with discrepancies between electrographic and radiological localizations had better outcomes when the resection was guided by imaging rather than EEG [22]. However, other authors believe that seizure-free outcomes are more likely in patients undergoing ‘standard’ epilepsy surgery rather than lesionectomy [127]. When complications of lesionectomy versus ‘standard’ cortical excision were compared, only one of 29 patients who underwent corticectomy had a persistent neurological deficit. In contrast, three of 21 patients with lesionectomy had similar deficits [18]. The presence of dual pathology may also modify outcomes. The best surgical results were achieved when the neocortical structural epileptogenic lesion and the abnormal medial temporal region were resected [15,68]. Three patients of Li et al. [68] became seizure-free after removal of both pathological regions while only two of 10 patients with single resections achieved the same favorable outcome.

5.5. EEG and ECoG patterns 5.5.1. Size of the epileptogenic zone and ability to establish its boundaries A large epileptogenic zone is the rule in ExT, especially in frontal epilepsy. Size is thought to be the main reason for surgical failure because complete excision cannot be accomplished [107]. Many authors have emphasized that only the best preoperative definition of location and size of the epileptogenic area can improve the surgical outcome [47,48,103]. 5.5.2. Morphology of ictal pattern Talairach et al. [116] reported that fast frequency ictal discharges on a scalp EEG is a good prognostic sign. Kazemi et al. [56] studied 17 patients with epilepsy secondary to head injury and showed that focal ictal b-frequency discharge was the only predictor of a seizurefree outcome. Wieser presented similar evidence when intracranial EEGs were recorded [128]. Others showed no correlation between morphology of ictal onset of ExT seizure and surgical outcome [60].

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5.5.3. Type of propagation of ictal activity In study of 26 patients with neocortical epilepsy, Kutsy et al. [60] showed that the type of seizure-spread influenced outcome. From among eight patients with slow contiguous spread, five (62.5%) became seizure-free, while only three of 13 patients (23%) with fast seizure propagation had a similar postoperative result. 5.6. Completeness of surgical resection Duchowny et al. [33] showed that in children undergoing epilepsy surgery, complete resection was the only significant prognostic factor. Optimum results were achieved only if the lesion (if present) and the electrographically defined epileptogenic zone were excised [48]. Rossi et al. [103] reported that resection of the lesion was more important that removal of the epileptogenic zone. However, the completeness of surgery is limited when the epileptogenic zone reaches functionally important, hence unresectable, cortex. Operations are also limited by imprecise localization of the epileptogenic zone.

6. Conclusion Epilepsy is no longer a single clinical entity because it shows a perplexing abundance of clinical symptoms and signs and abnormal electrophysiological and radiological features. Extratemporal epilepsy stands out as a fairly well-circumscribed disorder. However, it may be further divided into subtypes based on the site of seizure origin and the presence of etiological factors. Clinical semiology of the seizures may be helpful in establishing the type of epilepsy but is not always reliable. A number of clinical signs may allow correct lateralization and localization of seizure origins. Focal motor (‘Jacksonian’) seizures and attacks with characteristics of supplementary motor areas are likely to be of frontal onset. Seizures with sensory hemibody disturbances and simple visual alterations suggest an origin in the parietal and occipital lobes, respectively. Absence of ictal dystonic limb posturing and orofacial automatisms, fast progression to the clonic phase, ‘bizarre’ motor agitation, preservation of consciousness despite generalized motor activity, and rapid postictal recovery usually suggest an ExT origin. Interictal and ictal EEG patterns of ExT epilepsy are challenging due to their often misleading localizing features, paucity of changes, and unusual phenomena such as multifocal epileptiform discharges and secondary bilateral synchrony. Magnetic resonance imaging is an invaluable tool. If MRI defines a lesion, a surgical approach may prevail over medical management. The type of the lesion may help determine the likely outcome and predict the chance of surgical success. Neoplasms and vascular malformations suggest a favorable postoperative outcome. Lesions not shown by

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MRI, cerebral malformations, trauma, and the presence of ‘dual pathology’ imply worse postoperative results. Medical management of ExT epilepsy relies on monoor polytherapy with all currently available anticonvulsants. A surgical approach should be considered in all cases of medically intractable ExT epilepsy where a structural abnormality or well-delineated and excisable epileptogenic zone can be identified. When clinical, radiological, and electrophysiological findings are concordant, epilepsy surgery is more straightforward. When diagnostic methods produce conflicting observations, intracranial EEG monitoring is advisable. At any point during the work-up, surgery may be considered based on MRI findings alone (lesionectomy), although outcomes are usually better if a standard approach aimed at the electrophysiological definition of the epileptogenic zone is used.

Acknowledgements The author wishes to acknowledge the assistance of Dr A. Koeppen, review editor, in the completion of the manuscript.

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