The localizing value of the abdominal aura and its evolution

Methods.

We reviewed the database of our EEG video monitoring unit between July 1991 and December 1998 and identified 491 consecutive patients with focal epilepsies. All patients underwent noninvasive EEG video recording, which lasted between 3 and 18 days. Noninvasive EEG video monitoring was performed with closely spaced surface electrodes (10–10 system)14 and sphenoidal electrodes using 64- to 128-channel EEG machines (Vangard; Cleveland, OH). Additional invasive EEG video evaluations using stereotactically implanted depth electrodes (n = 8), subdural electrodes (strips or grids) (n = 8), or foramen ovale and epidural electrodes (n = 3) were performed in 19 patients who had abdominal auras. Interictal EEG discharges were counted and percentages of the different foci were calculated. The ictal EEG data were classified according to a system described in detail elsewhere.15 The seizures were analyzed by at least two epileptologists and classified according to a semiologic seizure classification, published in detail elsewhere.16,17⇓ The advantage of a semiologic seizure classification for the purpose of localizing seizures has been published recently.18 An abdominal aura was defined as an unnatural, eventually rising sensation of epileptic origin clearly localized to the epigastric or abdominal region. In the International League Against Epilepsy classification,19 it would be summarized under “simple partial seizure with autonomic symptoms or signs (including epigastric sensation, pallor, sweating, flushing)”. A seizure was classified as an automotor seizure if oral or manual automatisms were the most prominent feature. This seizure type corresponds best to “complex partial seizure with automatisms”according to the International League Against Epilepsy seizure classification.19 Although consciousness is impaired in most automotor seizures, there are well-documented exceptions to this rule in patients with nondominant temporal lobe seizure activity.20,21⇓

All patients underwent cranial MRI scan using proton-density weighted, T1-weighted, and T2-weighted images in axial, coronal, and sagittal planes (5-mm slices) (1.0 Tesla Impact/Siemens; Munich/Erlangen, Germany). If the routine MRI scan results were normal or surgical planning required additional tests, high-resolution MRI with three-dimensional fast low angle shot images (1- to 2-mm slices), inversion recovery technique, fluid-attenuated inversion recovery, or magnetization prepared rapid attenuated gradient echo was performed (1.5 Tesla Vision/Siemens; Munich/Erlangen, Germany 1.5 Tesla Gyroscan/Phillips, Best, the Netherlands). Further imaging studies in selected patients included interictal FDG-PET and ictal ECD-SPECT, performed according to protocols published elsewhere.22,23⇓ The epilepsy syndrome was defined in a case management conference (neurologists, neurosurgeons, neuroradiologists, neuropsychologists) based on the results of EEG, MRI, interictal FDG-PET, and ictal ECD-SPECT. For this study, seizure semiology was not used to define the epilepsy syndrome.

Statistical analysis was performed using the χ² test. A level of p < 0.05 was considered significant. The probability of underlying TLE was calculated with Bayesian analysis, taking into account that TLE was the most common epilepsy syndrome encountered in our epilepsy surgery centers.

Results.

Abdominal auras.

One hundred thirty (63 men and 67 women) of the 336 patients (39%) included in the statistical analysis had abdominal auras according to either patient history or EEG video monitoring. Their ages averaged 33 years (7 to 61 years). The mean age at onset of epilepsy was 13 years (1 to 41 years), and the mean duration of epilepsy was 19 years (0.5 to 55 years). Abdominal auras were more frequent in patients with TLE (117 of 223, 52%) than in patients with extratemporal epilepsy (13 of 113, 12%, p < 0.0001) (figure 1). Twenty-nine of the 155 patients (18.7%) in whom the seizure onset could not be localized to a particular lobe reported abdominal auras. Thus, based exclusively on the presence of an abdominal aura, the probability of TLE is 73.6% (54.7% for mesial TLE) (Bayesian analysis). The table summarizes the epilepsy syndrome, results of EEG video monitoring, MRI, and PET of the 13 patients with extratemporal epilepsy who had abdominal auras.

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Figure 1. Frequency of abdominal auras in temporal lobe epilepsy (TLE; n = 223) and extratemporal epilepsy (ETE; n = 113) patients in whom seizure onset was localized to one lobe. *** p < 0.0001. Black areas = abdominal aura; white areas = no abdominal aura.

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Table 1.

Seizure types and results of MRI, EEG, and PET of the abdominal aura of patients with extratemporal epilepsy

Abdominal auras were found in nine of 68 patients (13%) with frontal epilepsy, in 1 of 19 patients (5%) with perirolandic epilepsy, and in 3 of 18 patients (17%) with parieto-occipital epilepsy. These differences between extratemporal epilepsies were not significant.

Abdominal auras were more frequent in mesial (70 of 110 patients, 64%) than in neocortical TLE (16 of 41 patients, 39%, p = 0.007) (figure 2).

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Figure 2. Frequency of abdominal auras in mesial (n = 110) and neocortical temporal lobe epilepsy (TL; n = 41). ** p = 0.007. Black areas = abdominal aura; white areas = no abdominal aura.

No significant difference was found in the frequency of abdominal auras between right (69 of 130 patients, 53%) and left hemispheric epilepsies (61 of 130 patients, 47%) or between women (67 of 130 patients, 52%) and men (63 of 130 patients, 48%).

Evolution of the abdominal aura into other seizure types.

Abdominal auras were followed by automotor seizures in all patients with TLE (117, 100%). Two of these patients (2 of 117, 2%) experienced another aura before automotor seizures. One of these two patients had right neocortical TLE caused by an angioma. His abdominal auras evolved into auditory auras eventually followed by automotor seizures. The cause of epilepsy in the other patient was febrile convulsions. His MRI study showed right mesial temporal sclerosis. His abdominal auras were followed by somatosensory auras of the left hand, which evolved into automotor seizures. In contrast, abdominal auras were followed by automotor seizures in only two patients with extratemporal epilepsy (2 of 13 patients, 15%, p < 0.0001, figure 3) and in none of the 155 patients in whom the epileptogenic zone could not be localized to one lobe. Consequently, given the evolution of an abdominal aura into an automotor seizure, the odds of TLE are as high as 98.3% (mesial TLE, 37.0%). The table shows epilepsy syndrome and results of EEG video monitoring, MRI, and PET of the two patients with extratemporal epilepsy and the evolution of abdominal aura into automotor seizure (Patients 1 and 2). Patient 1 has perirolandic epilepsy secondary to encephalitis at the age of 8 years. He has an additional seizure evolution, which consists of somatosensory auras of the left arm evolving into automotor seizures. Patient 2 had frontal epilepsy with psychic auras following abdominal auras, which evolved into automotor seizures. He also had hypermotor seizures characterized by violent movements of the proximal extremities.

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Figure 3. Frequency of the evolution of abdominal auras into automotor seizures in temporal lobe epilepsy (TLE; n = 117) and extratemporal epilepsy (ETE; n = 13). *** p < 0.0001. Black areas = abdominal aura; white areas = no abdominal aura.

Abdominal auras were followed by tonic seizures in six of nine patients (66%) with frontal epilepsy. This evolution did not occur in patients with TLE. Two of nine patients with frontal epilepsy (22%) had psychic auras after an abdominal aura. Isolated abdominal auras occurred in one of the nine patients with frontal epilepsy (11%) and in one patient with parieto-occipital epilepsy (one of three patients, 33%). The other two patients with parieto-occipital epilepsy had unilateral clonic seizures after abdominal auras (two of three patients, 66%).

Discussion.

This study demonstrates analyzing the evolution of auras into other seizure types provides more localizing information than does the occurrence of a particular aura type. In our study, both mesial (70 of 110 patients, 64%) and neocortical TLE (16 of 41 patients, 39%) yielded significantly higher frequencies of abdominal auras than did any of the extratemporal epilepsies, namely frontal epilepsy (9 of 68 patients, 13%), perirolandic epilepsy (1 of 19 patients, 5%), or parieto-occipital epilepsy (three of 18 patients, 17%). Thus, the odds of correctly diagnosing TLE would be 73,6%, based exclusively on the occurrence of an abdominal aura. All but two studies on abdominal auras2,6⇓ limited their analyses to patients with either TLE9,11,12,24-27⇓⇓⇓⇓⇓⇓ or extratemporal epilepsy.10,28-33⇓⇓⇓⇓⇓⇓⇓ Our findings support these previous reports that abdominal auras are more frequently encountered in TLE (up to 67%) but also occur in extratemporal epilepsy (up to 22.5%), although less frequently.2,6⇓ Several auras (fear, olfactory, gustatory, experiential, and visual) have been found to differentiate between TLE and frontal epilepsies, but no localizing value for abdominal auras comparing frontal and temporal lobe epilepsy has been found.8 In contrast, a previous study7 did not find an association between the type of aura and the localization of “interictal cerebral dysfunction” documented by EEG.

There are several explanations for the differences in the frequency of abdominal auras in focal epilepsies. First, differing definitions of the abdominal aura may contribute to some discrepancies. Although some authors defined abdominal auras as purely epigastric or abdominal sensations,8,34,35⇓⇓ others also included throat or chest sensations.2,6⇓ Furthermore, abdominal auras are sometimes accompanied by fear,9,12,24⇓⇓ and some authors may have classified them as psychic or experiential auras. One study used a wide definition of “autonomic” auras and, therefore, might have included different aura types under this term.7 Another possible explanation for the differences in the frequency of abdominal auras in the literature could be caused by the data sampling. Postal questionnaires, used by several authors,7,8⇓ are subject to uncertainties. Many patients cannot recall particularly “minor” seizures.36 As the recollection of epileptic auras declines with increasing severity of the seizures,37 ictal testing during the aura and immediate postictal recollection in an EEG video monitoring unit, as in the current study, may be more reliable. Several authors7,9,25⇓⇓ correlated the occurrence of abdominal auras to the localization of “interictal EEG abnormalities” (epileptiform discharges and regional slowing), which usually is not sufficient to localize the epileptogenic zone.4 Localizing the epileptogenic zone is better in studies that use modern imaging techniques such as MRI or that are based on patients who were seizure-free after epilepsy surgery.2,12,13⇓⇓

Unlike some previous reports, which found a preponderance of right25,35⇓ vs left34 focal epilepsies with abdominal aura in TLE, no significant differences in right versus left focal epilepsies were found in our study. Our findings support those of most studies.2,6,9,24⇓⇓⇓

We found that analyzing seizure evolution is extremely helpful in distinguishing between TLE and extratemporal epilepsy. Automotor seizures followed abdominal auras in all patients with TLE who had abdominal auras (117, 100%). This evolution was observed in only two patients with extratemporal epilepsy and abdominal auras (p < 0.0001). The results of interictal and ictal EEG, MRI, and/or FDG-PET supported the diagnosis of extratemporal epilepsy in both these patients. Further analysis of seizure evolution showed that these two patients had additional seizure evolutions, which were not seen in the patients with TLE. Bayesian analysis shows that the chances of TLE are very high (98.3%) with an evolution of abdominal aura into automotor seizure.

Other studies on seizure semiology analyzed clusters of symptoms rather than the seizure evolution.8,27,35⇓⇓ Similar to our results, a previous study35 found a “tendency” toward the cluster of “epigastric aura, ictal vomiting, alimentary and hand automatisms”in TLE. A “strong relationship of epigastric sensation, subjective fear and motor behavior of the flight-fight pattern”in TLE has also been described before the era of imaging studies.26 In contrast, other authors8 described a significant correlation of oro-alimentary automatisms with “temporal lobe abnormalities” seen with imaging or EEG, but could not find a preponderance of abdominal auras in TLE or a localizing value for the combination of abdominal auras and seizures characterized by automatisms. In another study,27 a detailed cluster analysis of patients with TLE was performed, and subgroups, depending on the seizure onset zone, were described. Abdominal auras were not associated with a particular subgroup of TLE.27 The seizures were classified according to their most prominent feature in our study.38 Seizure classification was based on agreement of at least two independent observers (experienced epileptologists). Our method allows summarizing the main features of the seizure evolution, whereas less prominent features are not taken into account. The studies that applied cluster analysis used more variables and did not focus on the predominant ictal features, which may have contributed to the differing results.

The observation that abdominal auras are most frequently encountered in mesial TLE does not necessarily imply that mesial temporal structures are the symptomatogenic area for epigastric sensations.1 Stimulation of the anterior insular cortex in a recent study39 produced viscerosensitive and visceromotor responses similar to those obtained by temporomesial stimulation. Therefore, the authors suggest a visceral network of the anterior insula extending to the temporomesial structures. Up to 35% of patients who underwent anterior temporal resection for mesial TLE continued to have abdominal auras while otherwise seizure free.6,40⇓ These observations support the assumption that the symptomatogenic zone for abdominal auras is in the insular cortex.

Strong connections also exist especially between frontal/fronto-orbital areas and the anterior insular cortex. Thus, abdominal auras in patients with extratemporal epilepsies can be explained by the spread of seizure activity from clinically asymptomatic extratemporal brain areas. Demonstration of this phenomenon would require EEG registration of the seizure onset zone and the insular cortex with invasive electrodes. Invasive recordings of the insular cortex are technically difficult and rarely performed in epilepsy surgery. As with our patients, invasive electrodes did not cover the insular cortex.

Although the evolution of abdominal aura into automotor seizure was highly specific for TLE in our study, abdominal auras evolving into tonic seizures were the most common semiology in patients with abdominal auras who had frontal epilepsy (six of nine patients, 66%). Abdominal auras evolved into clonic seizures in two of three patients with parieto-occipital epilepsy (66%). These seizure evolutions were not observed in patients with TLE, again supporting the importance of analyzing seizure evolution to localize the epileptogenic zone.