Brain, Vol. 125, No. 10, 2320-2331,
October 2002
© 2002 Oxford University Press
Lateralizing semiology predicts the seizure outcome after epilepsy surgery in the posterior cortex
1 Bethel Epilepsy Center (Mara-Hospital) and 2 Epilepsy Research Foundation, Bielefeld, Germany
Correspondence to: Dr A. Ebner, Bethel Epilepsy Center (Mara-Hospital), Maraweg 21, D-33617 Bielefeld, Germany E-mail: ae{at}mara.de
Received January 22, 2002. Revised April 5, 2002. Accepted May 9, 2002.
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Summary |
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Compared with temporal or frontal resections, epilepsy surgery in the posterior cortex is rarely performed, and the literature concerning clinical predictors for the postoperative seizure outcome in this particular subgroup is sparse. The data of 42 patients with lesional focal epilepsies of the parieto-occipital lobe and the occipital border of the temporal lobe were evaluated retrospectively and related to the seizure outcome 2 years after epilepsy surgery. The investigated parameters included ictal semiology, pre- and postoperative EEG and neuroimaging, histological findings and demographic data. Postoperatively, seizure-free outcome was seen in: (i) 69% of patients with lateralizing auras, but only in 28% of patients without lateralizing auras (P = 0.01); and (ii) 57% of the patients with lateralizing seizures, but only in 17% of patients without lateralizing ictal semiology (P = 0.02). None of the patients with neither lateralizing auras nor lateralizing seizures achieved freedom from seizures (P < 0.01). The proportion of lateralizing seizures (P < 0.01) and auras (P = 0.02) in the total number of recorded seizures and auras was significantly related to the probability of a favourable surgical outcome. No patient with clinical lateralizing signs to the non-lesional hemisphere but 58% without such ‘false’ lateralization achieved freedom from seizures (P = 0.02). The following parameters also proved to be predictive for a favourable seizure outcome: (i) tumoural aetiology; and (ii) absence of epileptiform discharges in the postoperative EEG. The presence and frequency of ictal semiology lateralizing to the lesional hemisphere and the absence of lateralizing signs to the non-lesional hemisphere are highly predictive of a favourable outcome after surgical treatment of epilepsy in the posterior cortex.
Keywords: semiology; outcome predictors; epilepsy surgery; parietal; occipital
Abbreviations: DNT= dysembryoblastic neuroepithelial tumour; IED = interictal epileptiform discharge; MCD = malformation of cortical development; MST = multiple subpial transection; SP = seizure pattern
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Introduction |
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Epilepsies from the posterior cortex—namely the parieto-occipital lobes and the occipital border of the temporal lobe—account for the minority of focal epilepsies (Gibbs and Gibbs, 1952
; Rasmussen, 1991; Sveinbjornsdottir and Duncan, 1993). In patients with medically refractory epilepsies, the advent of more sophisticated neuroimaging methods along with improved electrographic monitoring also allowed for epilepsy surgery in the parieto-occipital lobes (Olivier and Boling, 2000; Geller and Heverly, 2001). On the other hand, posterior resections may lead to neurological deficits due to the relatively high proportion of eloquent cortex in this area (Rasmussen, 1969). Therefore, epilepsy surgery is carried out relatively rarely in the posterior part of the brain, compared with temporal or frontal lobe resections.
Identification of the epileptogenic region (Luders and Awad, 1991) in the pre-surgical diagnostic evaluation is usually performed by combining the data from ictal semiology, extra- or intracranial EEG and high resolution MRI (Ebner, 2001; Engel, 1996). Besides their role in delineating the cortical area to be resected, these data can also be used for predicting postoperative seizure outcome.
For mesial temporal lobe epilepsies (TLEs), the prognostic significance of interictal and ictal EEG propagation has been shown by several authors using scalp EEG (Hufnagel et al., 1994; Gilliam et al., 1997; Radhakrishnan et al., 1998; Schulz et al., 2000) and invasive EEG (Wieser and Siegel, 1991; Hufnagel et al., 1994; Holmes et al., 1997), respectively. Further predictors in TLE are preoperative MRI (Jack et al., 1992; Kuzniecky et al., 1993; Garcia et al., 1994; Berkovic et al., 1995), subclinical seizures and auras (Sperling and O’Connor, 1990), tumoural aetiology and normal intelligence (Gashlan et al., 1999). In frontal lobe epilepsies, the lack of generalized EEG signs (Janszky et al., 2000), the presence of preoperative MRI abnormalities and lack of contralateral head version (Ferrier et al., 1999) were shown to be significantly related to a favourable outcome.
In mixed series (temporal and extratemporal epilepsies), the following parameters have been shown to be prognostic for the outcome: extent of resection and pre-surgical seizure frequency (Rossi et al., 1999); interictal EEG activity and site of lesion (Dodrill et al., 1986; Guldvog et al., 1994; Armon et al., 1996; Bautista et al., 1999); slow contiguous spread of ictal activity in subdural EEG recordings (Kutsy et al., 1999); neuropsychological or psychiatric alteration (Dodrill et al., 1986); and duration of epilepsy, age at treatment, preoperative paresis and complex partial seizures (Guldvog et al., 1994). Where mentioned in these studies (Guldvog et al., 1994; Armon et al., 1996; Kutsy et al., 1999; Rossi et al., 1999), the proportion of patients with posterior epilepsies was 
6% of all investigated patients.
In accordance with the relatively low proportion of epilepsy surgery in the posterior cortex, the data concerning predictors in this particular subgroup are poor. However, the following parameters were shown to be correlated to a favourable outcome: lack of an ‘extralesional’ EEG focus (Blume et al., 1991; Bautista et al., 1999); early epilepsy onset (Blume et al., 1991); pure occipital resection and the absence of epileptiform discharges in the post-resection electrocorticographic or surface EEG (Salanova et al., 1992); and tumoural aetiology (Aykut-Bingol et al., 1998).
The aim of this study was to look for possible predictive factors for the postoperative seizure outcome by assessing preoperative test results of 42 patients who underwent epilepsy surgery in the posterior cortex. We focused on ictal semiology, electrophysiological data and the aetiology of epilepsy including histological findings.
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Methods |
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Patients
We retrospectively studied 42 patients (23 male) with lesional focal epilepsies of the posterior part of the brain. All patients were evaluated for epilepsy surgery at the Bethel Epilepsy Centre (Bielefeld, Germany) between 1991 and 1999. Resistance against at least two antiepileptic first line drugs was identified in all patients. The localization of the epileptogenic regions was distributed as follows: eight parietal, six occipital, two parieto-occipital, 21 lesions in the temporo-occipital and five in the temporo-parieto-occipital border (17 left, 25 right; the localization of each patient’s lesion is shown in the Appendix). Patients with additional epileptogenic regions outside the posterior cortex (e.g. mesial temporal sclerosis) were excluded. In our series, we did not exclude principally those patients with posterior lesions possibly involving speech-eloquent cortex from surgical intervention. However, in some cases, an involvement of Wernickes’ area led to incomplete resections in order to prevent postoperative speech deficits. In patients with left hemispheral lesions, the lateralization of speech and language dominance was tested by the Wada test and/or cortical stimulation with subdural grids (14 patients). In two patients, the left-sided cortical areas to be resected were clearly distant from the suspected language area, allowing a resection without prior testing for lateralization of speech dominance. In another patient with a widespread left temporo-parieto-occipital lesion, the dominance lateralization could not be performed due to mental retardation. In 10 patients with lesions involving the right temporo-parietal border (including the angular gyrus), the Wada test was used to exclude an unexpected right hemispheric dominance.
Age at surgery was 13.3–53.5 years (median 29.2 years), and duration of epilepsy was 3.2–43.5 years (median 19.9 years). Preoperatively, three patients (7%) had mild motor impairments, four (10%) had sensory deficits and six (14%) had visual field defects (including two patients with hemianopia). All patients underwent video and EEG monitoring with scalp EEG. Additional invasive EEG using subdural grids, epidural electrodes or depth electrodes was applied in 24 cases. All histories were gathered from standardized monitoring reports of the pre-surgical diagnostic phase. Epilepsy surgery was performed in all patients: 41 had cortical resection and one had a multiple subpial transection (MST). The histological diagnosis of the resected tissue was available for all patients and was correlated with the postoperative outcome.
Ictal semiology
All auras and seizures used for statistical analysis were recorded in the pre-surgical video EEG monitoring phase and were classified by at least two independent observers. In two patients, the lateralization of auras was achieved from their histories, as their auras in the monitoring phase were followed by complex focal or generalized tonic–clonic seizures with post-ictal amnesia. Altogether, 233 auras (0–37 per patient; median 5.6) and 566 seizures (0–65 per patient; median 13.5) were used for analysis. The ictal events were classified according to the semiological seizure classification (Luders et al., 1998). The following ictal semiology was considered lateralized: contralateral somatosensory (Siegel et al., 1999; Tuxhorn and Kerdar, 2000; Janszky et al., 2001) and visual auras (Williamson et al., 1992a; Anand and Geller, 2000); contralateral tonic, clonic or nystagmoid eye deviation (Williamson et al., 1992a); and contralateral tonic (Werhahn et al., 2000; Janszky et al., 2001), clonic (Noachtar and Arnold, 2000) or versive seizures (Rosenbaum et al., 1986; Wyllie et al., 1986; Quesney et al., 1990; Williamson et al., 1992b). Patients were considered to belong to the lateralized group if at least one aura or seizure could be clearly assigned to the lesional hemisphere. False lateralization was assumed if ictal semiology lateralized to the non-lesional hemisphere.
Neuroimaging
MRI using T1- and T2-weighted pulse sequences was available for all patients. The lesions were divided into the following subgroups: parietal, occipital, parieto-occipital, temporo-occipital and temporo-parieto-occipital (see Appendix). Both pre- and post-surgical MRI were compared to see whether the resection was complete or not. Two independent investigators (F.B. and R.S.) of whom one was blinded to the patients’ data (R.S.) performed the assessment of the MRI findings retrospectively. Moreover, 16 patients had interictal PET, and ictal SPECT (single photon emission computed tomography) was performed in three cases.
EEG data
All EEG data analysed in this study were recorded by superficial scalp electrodes placed according to the 10/10 system proposed by the American Electroencephalographic Society (1994). In some patients, sphenoidal electrodes were also placed. For the purpose of comparability, we did not investigate invasive EEG recordings in this study. The locations of interictal epileptiform discharges (IEDs) were assessed by visual analysis of interictal EEG samples of 2 min duration every hour. IEDs and ictal EEG were categorized with regard to their appearance in relation to the site of the lesion: (i) ipsilateral hemisphere; (ii) contralateral hemisphere; (iii) above the lesion; (iv) mirror focus; (v) temporal-anterior or mesial; (vi) frontal; (vii) central; or (viii) generalized. If the lesion involved the posterior temporal border, IEDs were only considered temporal if they were detected temporo-mesially and/or anterior. In some patients, intraoperative electrocorticography (ECoG) and/or electrical cortical stimulation was performed to determine precisely the cortical area to be resected. These intraoperatively collected electrophysiological data were not considered in this study. All EEG analysis was supervised by at least two board-certified electroencephalographers. Postoperative EEG was performed 6 months after the operation, and the data of 40 patients were available.
Histological findings
In every patient, the resected cortex was used for histological analysis. In one patient who had MST, a cortical specimen was taken for histological diagnosis. The findings of all patients were grouped as follows: cortical gliosis (e.g. due to trauma, encephalitis, ischaemic or haemorrhagic processes); dysembryoplastic neuroepthelial tumour (DNT); glioma (gangliogliomas, oligodendrogliomas, astrocytomas IIo WHO); discrete vascular lesions (arteriovenous malformations, cavernoma, etc.); and all kinds of malformations of cortical development (MCDs). None of the patients had WHO IIIo or IVo tumours.
Surgical outcome
We divided the patients into two groups according to the outcome of their surgery—those who had no seizure at all (except auras) following surgery (Engel Ia and Ib), and those with persistent seizures (Engel Ic–IV; Fig. 1). The follow-up period was at least 2 years. The outcome was assessed after 2 years, using Engel’s classification (Engel, 1987).
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Statistical analysis
Fisher’s exact test was used; P values <0.05 were considered as significant. Furthermore, logistic regression was used to calculate the predictive value of each lateralized ictal event for the surgical outcome by using the following equation:
Prob (event) = 1/(1 + e–Z)
Prob (event) is the estimated probability of becoming seizure free dependent on the proportion of lateralizing seizures and auras (Z):
Z = B0 + B1[n(LS)/n(s)] + B2[n(LA)/n(A)]
The proportions of lateralizing seizures n(LS) and auras n(LA) referring to the total number of the detected seizures n(S) or auras n(A) were used as the independent variables; the regression parameters B0, B1 and B2 were estimated by logistic regression procedure. All statistical analyses were carried out with the SPSS statistical package for Windows (SPSS Inc., Chicago, IL, USA).
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Results |
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Result of surgery
Nineteen of the 42 patients included in this study were free of seizures after 2 years, although the majority of patients improved (Fig. 1). Twenty-three patients (55%) developed predictable surgery-related deficits: most frequently (45%, n = 19 out of 42) visual field defects. Four of six patients with occipital lobe resections developed a hemianopia, and 11 of the 21 temporo-occipital resected patients had surgically related scotomas, of which five were hemianopias. Two patients developed moderate contralateral sensimotor deficits after multiple lobe resections. Seven per cent (n = 3) had contralateral sensory deficits, all of them had resections involving parietal structures. These sensory deficits did not lead to a significant impairment of the patients’ daily activities. There were no major complications due to surgery, but two patients died after the follow-up period (one committed suicide and one died due to traumatic intracranial bleeding not related to the operation). In general, most of the predictable post-surgical deficits were minor (except hemianopia).
Ictal semiology
There was a great variety of aura and seizure types, without any of them significantly indicating particular cortex regions. In addition to the frequently observed semiology listed in Table 1, there were some rare ictal events, detected in fewer than a quarter of the patients: auditory auras (three patients), abdominal auras (10 patients), gustatory auras (two patients), atonic seizures (one patient) and hypermotor seizures (three patients). Generalized tonic–clonic seizures were seen in 34 of the 42 patients. There was no significant correlation between the number of different seizure types and the surgical outcome. In addition, there was no correlation between the occurrence of generalized tonic–clonic seizures and the outcome after surgical treatment.
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Lateralization to the lesional hemisphere
Sixteen patients had a total of 93 lateralizing auras assigned to the lesional hemisphere (1–37 per patient; median 7). Sixty-nine per cent (n = 11 out of 16) of those were seizure free. In contrast, only 28% (n = 7 out of 25) of the patients without lateralizing auras achieved freedom from seizures (P = 0.01). Of the 566 seizures recorded, 158 were lateralized and could be seen in 30 patients (median 2; range 0–33). Fifty-seven per cent (n = 17 out of 30) of those patients with lateralized seizures but only 17% (n = 2 out of 12) of the patients without lateralized seizures were seizure free after surgery (P = 0.02, see Fig. 2). Combining auras and seizures revealed that none of nine patients with only non-lateralizing semiology was seizure free, while 48% (n = 9 out of 19) with either lateralizing auras or lateralizing seizures and 69% (n = 9 out of 13) of those with both lateralizing auras and lateralizing seizures were free of seizures (P < 0.01, see Fig. 2). Logistic regression showed that the proportion of lateralizing seizures (P < 0.01) and auras (P = 0.018) in the total number of recorded seizures and auras was significantly related to the probability of a favourable surgical outcome. Seventy-four per cent (n = 14 out of 19) of the seizure-free group and 87% (n = 20 out of 23) of the non-seizure-free group were estimated correctly (r2 = 0.409; see Fig. 3). The correlation between lateralizing semiology and seizure outcome remained significant even if patients with a tumoural aetiology, which itself proved to be related to freedom from seizures, were not considered: in the non-tumoural group, the P value for auras was 0.019 and for seizures 0.01.
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Lateralization to the non-lesional hemisphere
None of the nine patients with lateralizing signs to the non-lesional hemisphere, but 58% (19 out of 33) without such ‘false’ lateralization attained freedom from seizures (P = 0.02). Moreover, it could be shown that all patients (n = 8 out of 8) without false lateralization but with both lateralizing auras and lateralizing seizures were free of seizures (P < 0.01).
EEG findings
Interictal epileptiform discharges (IEDs)
In 38 patients (90%), IEDs were found. Twenty five of those 38 patients (66%) had regionalized IEDs over the site of lesion, which was not significantly associated with the seizure outcome (P = 0.3). A spread of IEDs into temporal structures was seen in 20 of the 38 patients (52%): 11 patients (29%) only ipsilateral temporal, seven patients (18%) ipsi- and contralateral and two patients (5%) only contralateral temporal. Over the frontal cortex, IEDs were detected in 13 patients (34%): seven patients (18%) only ipsilateral frontal, three patients (8%) ipsi- and contralateral and again three patients only contralateral frontal. There was no relationship between the appearance of IEDs in any cortical region and the surgical outcome.
Seizure patterns (SPs)
In 40 of the 42 patients (95%), SPs could be recorded in the non-invasive EEG. Twenty-five patients had SPs over the site of the lesion. In five patients, the contralateral posterior cortex was involved in the EEG-onset zone. Of those, one patient with a lesion involving the right lateral and mesial occipital cortex (patient 9 in the Appendix) had SPs over the ipsi- and contralateral occipital cortex. In the remaining four patients (10%) with occipito-lateral (patient 10), occipito-lateral and mesial (patient 12) or temporo-occipital lesions (patients 32 and 34), the ictal onset of the EEG was detected exclusively in the same but contralateral region. There was a tendency for SPs outside the lesion to be associated with worse seizure outcome: nine of 14 patients (64%) with SPs arising only from cortical regions that are involved in the resected region had a complete cessation of seizures. Of those 27 patients with SPs arising from cortical regions distant from the lesion or with a generalized SP, only nine (33%) achieved freedom from seizures (P = 0.059). The isolated occurrence of an initially generalized SP led to a persistence of seizures in six of seven patients (86%), whereas the absence of generalized SPs led to this in 16 of 33 patients (49%; P = 0.081).
Postoperative EEG findings
Twenty-one of the 40 patients with available postoperative EEG data (53%) showed a persistence of IEDs in the EEG 6 months after the operation. Of these patients, 71% (n = 15) were not seizure free after 2 years, whereas 12 of 19 patients (63%) without postoperative IEDs were seizure free (P = 0.03). There was no significant correlation between the completeness of resection and the appearance of postoperative IEDs (P = 0.6).
Aetiology of epilepsy
All patients had defined lesions in pre-surgical MRI, which could be identified histologically as tumours in 10 cases: ganglioglioma (n = 4), oligodendroglioma (n = 2), DNT (n = 3) and astrocytoma IIo WHO (n = 1). In 32 patients, a non-tumoural aetiology was found: MCD (n = 10), discrete vascular lesions (arteriovenous malformations, cavernoma, etc.; n = 5) and cortical gliosis (n = 17). Eighty per cent (n = 8 out of 10) of the patients with a tumoural aetiology but only 34% (n = 11 out of 32) of the non-tumoural group were seizure free after the operation (P = 0.015; see Fig. 4).
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Completeness of resection by postoperative MRI
Twenty-three patients had a complete resection of their lesion, while 18 patients could not be resected completely. One patient had MST, which did not lead to freedom from seizures. In five patients, the incompleteness of resection was caused by an extension of the lesion into the posterior speech area. Another patient with a lesion susceptibly involving Wernickes’ speech area was also resected incompletely. In this patient, a prior lateralization of speech dominance was impossible due to mental retardation. We found a slight tendency for a favourable outcome if there was a complete resection of the lesion seen on pre-surgical MRI, but the data did not reach significance (P = 0.29). The proportion of complete resections did not differ significantly between the different aetiologies: 60% of the tumoural lesions (n = 6 out of 10), 60% of the vascular lesions (n = 3 out of 5), 50% of the gliotic lesions (n = 8 out of 16; one also had MST) and 60% of the MCDs (n = 6 out of 10) were completely resected. Focusing on the tumoural group, the number of seizure-free patients after complete resections was markedly higher compared with other aetiologies: All of the six patients with complete tumourectomies but only 50% of the incompletely resected patients (n = 2 out of 4) attained freedom from seizures. However, the number of patients in this subgroup is too small for formal statistical analysis. Furthermore, there was no correlation between the number of cortical lobes involved in the resection and the outcome.
Demographic data
No significant correlation could be shown between the seizure outcome and the following data: (i) age of epilepsy onset; (ii) duration of epilepsy; (iii) age at surgery; (iv) amount of pre-surgically tested antiepileptic drugs; (v) pre-existing status epilepticus from the patients’ histories; and (vi) pre-existing neurosurgical but not epilepsy surgical procedures.
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Predictors for the seizure outcome
Ictal semiology and auras
As a main result of our retrospective study, we showed the presence and frequency of ictal semiology, either auras or seizures, lateralizing to the side of the lesion to be highly predictive for a favourable seizure outcome. The presence of both lateralized auras and lateralized seizures predicted the highest rate of freedom from seizures. In addition, we could show that auras or seizures lateralizing to the contralateral side of the lesion predict the persistence of postoperative seizures. As the evaluation of clinical lateralizing signs in video EEG monitoring has a high reliability (Chee et al., 1993
), our findings reveal a more or less easily assessable parameter for pre-surgical prognostic considerations. Pathophysiologically, the presence of lateralizing auras suggests a circumscribed ictal activation of eloquent cortex lasting long enough to produce subjective perception of, for example, somatosensory or visual sensations. Several factors may be taken into account for the explanation of non-lateralizing or absent auras such as more widespread epileptogenic zones or more rapid spread to ipsi- and contralateral brain regions due to less developed mechanisms of suppressing propagation or an epileptogenic zone localized in mesial instead of lateral cortex. The lateralizing ictal motor signs indicate spread of seizure activity within the same hemisphere to frontal motor areas with no or only late involvement of the contralateral side. Non-lateralizing or ‘false lateralizing’ ictal semiology may reflect rapid seizure spread to both hemispheres or predominantly to the contralateral hemisphere. However, bilateral epileptogenicity also cannot be completely excluded in those cases.
In contrast to the strong association between lateralizing semiology and seizure outcome, the localizing value of ictal semiology was poor. However, the presence of somatosensory and visual auras is observed regularly in epilepsies arising from parietal and occipital regions (Schulz et al., 1997; Tuxhorn and Kerdar, 2000). As can be seen in Table 1, lesions involving the occipital cortex regularly were associated with visual auras (n = 24 out of 34, 71%), whereas a strictly parietal lesion was found in only one patient with visual auras. Elementary visual auras occurred in six of 10 patients (60%) with lesions involving the mesial and in eight of 18 (44%) with lesions involving the lateral occipital cortex, but could only be detected in 31% of the cases with lesions in the temporal–occipital junction. These findings are consistent with recently published data (Bien et al., 2000). These authors showed elementary visual auras in 44% (n = 4 out of 9) of their occipital group and in 33% (n = 2 out of 6) of their temporo-occipital group. Complex visual auras were reported only if the temporal lobe was involved in the lesion. This could be reproduced by our findings, as the majority of our patients with lesions in the lingual gyrus (64%, n = 7 out of 11) and half of the patients (n = 5 out of 10) with lesions in the fusiform gyrus experienced complex visual auras. On the basis of depth electrode recordings, those observations previously have been interpreted by several authors as a phenomenon of spreading into limbic structures (Jones and Powell, 1969; Babb et al., 1981; Olivier et al., 1982; Williamson et al., 1992a; Palmini et al., 1993). This is in accordance with our findings, as all of our patients with complex visual auras also developed complex partial seizures. The lateralizing aspect of this aura type was first described by the Montreal group (Salanova et al., 1992). The authors reported four out of 42 patients with occipital lobe epilepsies having visual hallucinations as an aura. All four patients had right occipital lesions. This predominance of the right side could be reproduced by our findings as all of our five patients with complex visual auras had right-sided epileptogenic lesions too. However, a significant relationship to the outcome in this particular subgroup could not be proved.
Somatosensory auras occurred in seven of our nine patients with a lesional involvement of the parietal lobe. Our data could not confirm previously published data of Bergen et al. (1984), showing elementary sensory auras to be associated with worse seizure outcome. In our series, four of six patients with lateralized, but none of the three with non-lateralized somatosensory auras had a complete cessation of seizures.
EEG findings
In our series, we found a frequent propagation of epileptiform activity, namely IEDs and ictal SPs, into cortical regions outside the area harbouring the lesion. Thus, delineation of the epileptogenic region could not always be achieved by scalp EEG so that invasive EEG recordings were necessary in 24 cases. Our observation of multifocal epileptiform activity in the scalp EEG coincides well with other studies dealing with EEG phenomena recorded from posterior areas (Ludwig and Marsan, 1975; Salanova et al., 1992, 1995a; Williamson et al., 1992a, b; Cascino et al., 1993; Palmini et al., 1993; Foldvary et al., 2001). The rate of regionalized SPs in our series was higher in patients with MCDs than in patients with cortical tumours. This is in accordance with the findings of Aykut-Bingol et al. (1998) who found occipital IEDs in 17% of all their patients, but in 29% of those patients with MCDs. SPs were reported in 50% of their cases with MCD but almost never in patients with cortical tumours. The authors could not show any relationship between occipital versus extraoccipital EEG findings and seizure outcome.
In our series, the lack of extralesional or generalized SPs was correlated to a favourable seizure outcome, although the data did not reach significance. This observation has been published previously for posterior epilepsies (Blume et al., 1991) and frontal lobe epilepsies (Janszky et al., 2000). In contrast to temporal lobe epilepsies, where the lack of contralateral IEDs is highly predictive for a seizure-free outcome (Schulz et al., 2000), we could not prove this correlation for posterior epilepsies.
Our data significantly confirmed the prognostic value of remaining IEDs in the postoperative EEG (P = 0.03), which has been shown previously for occipital lobe epilepsies (Salanova et al., 1992) and temporal lobe epilepsies (Godoy et al., 1992). The correlation between postoperative IEDs and surgical outcome may reflect the persistence of epileptogenicity in the remaining cortical tissue. However, six patients achieved freedom from seizures, although IEDs were still seen in the postoperative EEG. In these cases, the IEDs may reflect the persistence of epileptogenicity in discrete cortical areas. Probably a spread of epileptogenic activity from these discrete areas is prevented due to the cortical resection. Furthermore, we found no significant correlation between the completeness of resection and the appearance of postoperative epileptiform discharges in the EEG. Therefore, it can be speculated that the remaining epileptogenicity may arise from cortical areas that are not necessarily part of the MRI-definable lesion. In the course of epilepsy, this irritative zone (Luders and Awad, 1991) outside the lesion may have developed a secondary epileptogenicity, which may account for the persistence of seizures in those patients in whom epileptogenic lesions could be removed completely.
Aetiology
Malformation of cortical development (MCD). Since 1971, when Taylor first described MCD as an aetiology for focal epilepsies (Taylor et al., 1971), MCDs have been diagnosed increasingly in epilepsy surgical series (Andermann and Guerrini, 1996). In our study, 10 patients had MCDs, and four of them were seizure free after resection. This observation supports previously published data of Aykut-Bingol et al. (1998) who reported 45% of their patients with occipital developmental malformation becoming seizure free after epilepsy surgery. The authors concluded that the presence of developmental malformations is of some prognostic significance regarding seizure outcome. Kuzniecky et al. (1997) evaluated nine patients after resections of occipital MCDs. Three of those patients achieved freedom from seizures, and the remaining seven patients improved. In a mixed series of 35 mainly frontal and temporal lobe epilepsies, 49% of patients with MCDs were seizure free (Edwards et al., 2000). One possible reason for the relatively poor outcome in patients with MCD may be a greater extent of the malformation outside the resection site. Several studies showed that the whole extent of dysplastic cortex is identifiable only infrequently by MRI (Kuzniecky et al., 1991; Chugani et al., 1993; Otsubo et al., 1993; Raymond et al., 1995; Tassi et al., 2001).
Cortical tumours. Eight of our 10 patients with tumoural aetiology were seizure free after resection. The outcome was significantly better in the tumour group if compared with non-tumoural aetiologies (P = 0.015). This supports the findings of Aykut-Bingol et al. (1998), who found that 77% of their occipital tumour patients but only 27% of their patients with a non-tumoural aetiology became seizure free. In temporal lobe epilepsies, the correlation between tumoural aetiology and postoperative freedom from seizures has been described by Gashlan et al. (1999). It can be assumed that resections of non-malignant cortical tumours with proven epileptogenicity belong to that group of epilepsy surgery interventions with the highest benefit for the patient’s seizure outcome. Our data indicate that it is even more beneficial if the tumour can be removed completely since all six patients with complete but only two of four patients with incomplete tumourectomies attained freedom from seizures.
Vascular malformations. One possible reason for the relatively poor outcome in our angioma and cavernoma group (only one of five patients was seizure free) may be that the seizure history was longer than 5 years in all patients with vascular malformations. Previous studies showed epilepsy lasting longer than 1 year to be associated with the persistence of postoperative seizures in patients with arteriovenous malformations (Yeh et al., 1993) and cavernomas (Cohen et al., 1995), respectively.
Variables with no significant predictive value
Seizure-free outcome tended to be more frequent among patients who had a complete resection based on postoperative MRI (12 out of 23, 52%), compared with patients with incomplete resections (7 out of 18, 44%), but the difference was not significant. This is consistent with the findings of Edwards et al. (2000) in their 35 patients with MCD, but contrasts with the data of Blume et al. (1991), who found that two of their five patients without any seizure improvement were resected incompletely. In addition, the authors reported the age of epilepsy onset to be predictive for seizure outcome, which is in contrast to our findings. None of our data, obtained from the patients’ history, could be correlated to the outcome.
General outcome
Epilepsy surgery in the posterior cortex is rarely performed compared with temporal or frontal resections. In our epilepsy surgery programme, parieto-occipital resections accounted for 8% of all resections in adults between 1990 and 1999. The relatively high proportion of patients who benefited from this surgery (80%), in particular those who achieved freedom from seizures, proves the reliability of epilepsy surgery even in the posterior cortex. However, the relatively high incidence of surgery-related neurological impairments has to be taken into account. The latter reflects the general problem of cortical resections in regions with a high proportion of eloquent cortex.
Reports from the literature (see Table 2) show differences in the outcome after epilepsy surgery in the posterior cortex. However, the data are hardly comparable due to differences in follow-up periods ranging from 0.3 to 50 years, different outcome classifications and partly focusing on particular subgroups (e.g. pure tumour resections).
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Conclusion
The presence and frequency of ictal semiology lateralizing to the lesional hemisphere and the absence of lateralizing signs to the non-lesional hemisphere are highly predictive of a favourable outcome after surgical treatment of epilepsy in the posterior cortex. Our findings underline the great importance of the correct classification of epileptic auras and seizures in pre-surgical diagnosis.
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Acknowledgements |
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The authors wish to thank the members to the epilepsy monitoring unit of the Bethel Epilepsy Center, especially Dr Heinz Pannek who carried out most of the operations on our patients, and Professor Rainer Lahl and Dr Rafael Villagran for the neuropathological evaluation of the surgical specimens. This study was supported by a grant from the German Research Council (DFG EB111/2-2).
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Schematic diagram illustrating the anatomical localization and extension of each patient’s lesion (black area): cases 1–8, parietal lesions; cases 9–14, occipital lesions; cases 15 and 16, parieto-occipital lesions; cases 17–37, temporo-occipital lesions; cases 38–42 temporo-parieto-occipital lesions.APPEN
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