Benign Focal Seizures of Adolescence: A Prospective Study
Address correspondence and reprint requests to Dr. R.H. Caraballo at Neurología, Hospital de Pediatría “Prof. Dr. Juan P Garrahan,” Combate de los Pozos 1881, CP 1245, Buenos Aires, Argentina. E-mail: email@example.com
Summary: Purpose: To characterize the clinical and EEG findings and evolution of the syndrome of benign focal seizures of adolescence (BFSA), as described by Loiseau et al.
Methods: A prospective study was performed in adolescents with normal clinical and neurologic examinations and normal neuroradiologic studies who had focal seizures that occurred isolated or in a cluster, with or without secondary generalization in the first 24 to 48 h after onset. None of the patients was treated with antiepileptic drugs (AEDs).
Results: Between January 1996 and January 2002, 15 patients with BFSA were enrolled in the study. Median age at onset of BFSA was 14 years. Thirteen patients had focal sensory or motor seizures. In two patients, the ictal manifestation was motion arrest associated with oral automatisms. Eight of them evolved to generalized tonic–clonic seizures. Thirteen patients had seizures only when awake, and the other two, both when awake and during sleep. Repeated interictal EEGs were normal, but in four of the patients who had seizures in a cluster, we were able to record an EEG within 8 h after seizure onset. Two of these four patients had focal seizures, and their waking EEG showed focal centroparietal theta activities. The other two patients had secondarily generalized seizures, and their waking EEG showed bilateral theta activities instead. Prognosis was excellent.
Conclusions: BFSA is a well-defined seizure syndrome, recognizable by clinical and EEG features, as described by Loiseau et al. In teenagers with these electroclinical features with a normal neurologic examination and normal neuroradiologic findings, AEDs should be avoided.
In 1972, Loiseau et al. (1) reported a series of 14 patients with unprovoked isolated focal seizures in adolescence who were followed up for 4 to 12 years. In a later study, Loiseau and Orgogozo (2) described 83 adolescents with these features and concluded that the entity is not an epilepsy syndrome, but a seizure-susceptibility syndrome.
In 2002, the series was updated and increased to 108 cases followed up for ≥5 years (3). Few other studies of patients with focal seizures of adolescence have since been published (4–9).
Benign focal seizures of adolescence (BFSA) is a transitory condition occurring predominantly in male subjects, starting in the second decade of life, with a peak of onset between ages 13 and 14 years. BFSA is characterized by simple focal motor and somatosensory seizures with secondary generalization occurring isolated or in a cluster in the first 24 to 48 h after onset. The seizures happen predominantly when the patient is awake and have a benign course. The interictal EEG, neurologic examination, and neuroradiologic images are normal, and a family history of epilepsy is rare (10).
Ours is a 6-year prospective study of 15 patients with BFSA.
This study was set up at the Department of Neurology of our hospital in January 1996. Strict inclusion criteria comprised adolescent patients with focal seizures that occurred isolated or in a cluster, with or without secondary generalization during the first 24 to 48 h after onset, with normal neurologic and mental examination and normal brain imaging. A normal interictal EEG was not considered to be a strict inclusion criterion.
The age cutoff of the first unprovoked seizure was from 11 to 18 years. None of the patients received treatment with antiepileptic drugs (AEDs). Patients with known mental or neurologic deficits or neuroradiologically documented lesions were excluded. We also excluded patients with a diagnosis of generalized epilepsy, benign childhood epilepsy with centrotemporal spikes (BCECTS), or childhood epilepsy with occipital paroxysms (CEOP) (11,12).
We analyzed gender, age at onset, personal and family history of epilepsy or febrile convulsions, duration, manifestation, circadian distribution, frequency of seizures, and evolution.
EEGs were performed while the patients were awake and asleep. However, ictal EEGs could not be recorded. Electrodes were placed according to the International 10-20 system. All patients underwent brain computed tomography (CT) scans, and six underwent magnetic resonance imaging (MRI). All results were normal.
All patients were evaluated longitudinally, clinically, and by EEG. Repeated EEG recordings were obtained in all patients every 3 to 6 months. Clinical and EEG details of all patients were reviewed and unanimously agreed on by all authors.
Number of patients and gender
Fifteen patients, 10 boys and five girls, met the inclusion criteria for BFSA in a 6-year period (January 1996 to January 2002). In the same period, we also registered 17 patients with late-onset benign focal epilepsy of childhood (11 with rolandic spikes and six with occipital spikes), eight patients with cryptogenic focal epilepsy, and 38 patients with symptomatic focal epilepsy. The eight patients with cryptogenic partial epilepsy were easily excluded, as they had more polymorphous and often complex partial seizures without secondary generalization. Neurologic, neuroradiologic, and intellectual normality was found, but the seizures were frequently refractory to AEDs.
Age at onset
The age at onset of the seizures ranged from 11 to 18 years, with a mean age of 13.5 and a median age of 14 years.
Personal and family history of febrile convulsions and epilepsy
A family history of epilepsy was found in one patient. None of the patients had a personal and/or family history of febrile convulsions.
Simple focal seizures occurred in 13 (86.6%) and were characterized by eye and/or head deviation in five, facial tonic or clonic focal seizures in five, and visual symptoms followed by upper extremity clonic focal seizures in three. Seizures were followed by tonic–clonic seizures with secondary generalization in seven. The motor seizures were not followed by a jacksonian walk. In 11 patients, motor seizures were followed by focal numbness with or without a jacksonian walk. In two patients, seizures presented as motion arrest and oral automatisms, followed by tonic–clonic seizures with secondary generalization in one. According to parental report, the duration of seizures was ∼2 min, but in patients who had secondarily generalized seizures, they lasted ∼5 min.
All 15 patients had seizures when awake, and two of the four patients who had seizures in a cluster also had seizures during sleep.
Frequency of seizures
The event was a single seizure in 11 (73.3%) patients. In the remaining four, a cluster of two to four seizures occurred in <48 h.
All 15 patients had a normal interictal EEG at onset, and repeated control EEGs when awake and asleep were normal as well. In the four patients who had seizures in a cluster, we were able to record an EEG within 8 h after the seizures. Two of these patients had focal seizures, and the awake EEG revealed focal centroparietal theta activities. In the other two who had secondarily generalized seizures, it showed bilateral theta activities instead.
By definition of the inclusion criteria, patients did not receive AED treatment.
During a follow-up period ranging from 2 to 6 years (mean, 4.5 years) no recurrence was noted. The electroclinical features and evolution of the patients are summarized in Table 1.
Table 1. Electroclinical features and evolution of our series of patients
|1||11||M||SPS/SG||R hand jerking, followed by limb numbness||−||N||No|
|2||15||M||SPS/SG||Eye and head deviation||−||N||No|
|3||12||F||SPS||Phosphenos followed by arm jerking and numbness||Yes||FC-PTA||No|
|4||14||M||CPS||Motion arrest followed by oral automatism||−||N||No|
|5||15||F||SPS/SG||Head deviation followed by limb numbness||−||N||No|
|6||15||F||SPS||Eye and head deviation followed by facial numbness||−||N||No|
|7||14||M||SPS/SG||Face tonic seizure followed by shoulder numbness||Yes||BC−PTA||No|
|8||14||M||SPS||R arm jerking, followed by limb numbness||−||N||No|
|9||16||F||SPS||Face clonic seizure followed by limb numbness||−||N||No|
|10||11||M||SPS/SG||Head deviation followed by facial numbness||−||N||No|
|11||12||F||SPS||Visual symptoms followed by R arm jerking||−||N||No|
|12||11||M||CPS/SG||Motion arrest and oral automatism followed by SG||−||N||No|
|13|| 14.5||M||SPS/SG||Phosphenos followed by arm jerking and numbness||−||N||No|
|14||17||M||SPS||Face clonic seizure followed by limb numbness||Yes||FC-PTA||No|
|15||11||M||SPS/SG||Eye and head deviation followed by shoulder numbness||Yes||BC-PTA||No|
This is the first prospective study on this solitary seizure event that may occur once in a lifetime or very rarely, at lengthy intervals (7). BFSA may represent between 6 and 25% of focal epilepsies in adolescents between ages 11 and 19 years (4–9). In our series of patients, BFSA affected 19% of adolescents with focal epilepsies. However, no population-based study documents these figures.
Our series of patients predominantly had isolated motor or somatosensory focal seizures, occurring as a single event or in a cluster, in a short period of ≤48 h. Two patients had isolated complex partial seizures, in one of them followed by secondarily generalized tonic–clonic seizures. In these two patients, a longer follow-up is necessary to confirm a benign course, as typically occurs in BFSA. The repeated EEG recordings when awake and asleep were always normal, as was demonstrated by us in a previous retrospective study (6). Similar EEG findings in patients with BFSA were initially described by Loiseau et al. (2). However, King et al. (7) and Capovilla et al. (9) found unilateral or bilateral theta activities predominantly during sleep, as we did in the four patients with seizures occurring in a cluster but when awake. This latter author also found posterior spikes in 10 of their 37 patients (9). The absence of a family history of febrile seizures or epilepsy was another finding in our series that coincided with the series of Loiseau et al (3). Conversely, Capovilla et al. (9) found a high rate of family history of epilepsy, supporting a probable idiopathic nature. In Table 2, the series of patients with BFSA that have been published are described.
Table 2. Series of patients with BFSA published
|Loiseau et al. (2002) (108 patients)||71.2%||Peak at 13–15||87.4%||13.6%||57.2%||87%||13%||Normal|
|Capovilla et al. (2001) (37 patients)||60%||Mean,14.5||86%||27%||57%||62%||38%||Spikes, sharp waves and theta discharges|
|Mauri et al. (1996) (10 patients)||70%||Range,12–19||30%||20%||50%||?||?||Unspecified abnormalities|
|King et al. (1999). (8 patients)||50%||Mean age,15.5||100%||-||75%||?||?||Unspecified abnormalities|
|Caraballo et al. (1999).||71.4%||Peak at 12–13||85.7%||26.7%||64.2%||93%||7%||Normal|
| Retrospective study (14 patients)|
| Prospective study (15 patients)||66.5%||Median,14||86.6%||13.4%||40%||100%||13.3%||Normal or unspecified abnormalities|
In an adolescent patient with a first unprovoked focal seizure, the possible presence of an underlying brain lesion should be suspected, and a poor prognosis considered. Consequently, a brain MRI should always be performed in these patients. A high expectation of seizure recurrence exists, even when neuroradiologic imaging is normal, and a diagnosis of cryptogenic focal epilepsy is possible in the absence of a brain lesion. However, this study confirms that a benign course may be seen in adolescents with focal seizures, normal neurologic examination, and normal brain imaging. It is crucial to identify this condition to avoid giving a poor prognosis at a first seizure, only because this type of seizure occurred during adolescence. AED treatment should be avoided in these cases, as the course is benign and the seizures isolated. Naturally, the evolution of the patient will confirm the diagnosis of this entity.
As Loiseau et al. (3) very rightly remarked, we should ask ourselves whether the first diagnosed seizure is really the first experienced seizure. Generalized seizures are easier to recognize, but a brief focal seizure can be less impressive and more difficult to identify. Thus it is very important in our practice to take a detailed interview from both the parents and the teenager.
The pathophysiology of these focal seizure events is still a challenge for epileptologists. Longer follow-ups and future prospective electroclinical studies are necessary to confirm and define the nosologic place of this entity.
The most important differential diagnosis of BFSA is cryptogenic focal epilepsy, in which a normal neurologic examination and normal neuroradiologic imaging are often found. Electroclinical features and evolution in patients with focal cryptogenic epilepsy are different from those found in our benign cases. Late-onset benign focal epilepsy of childhood, like BCECTS or CEOP, also may be considered as a differential diagnosis. Patients with migraine may present a sensory march without motor seizures. However, none of the patients in our series had migraine.
In conclusion, this prospective study confirms the existence of adolescents with isolated focal motor or somatosensory seizures, and less frequently other focal seizure types, with or without secondarily generalized seizures, with a normal EEG, normal neurologic examination, normal brain imaging, and a benign course, as previously described by Loiseau et al. (2).
In adolescents with a first appearance of these electroclinical features and with normal neurologic examination and normal neuroradiologic findings, AED treatment should be avoided.
Whether the patients described here represent an epileptic syndrome or merely had a single seizure event with a normal interictal EEG should be discussed.